Abstract
This chapter summarizes the multiple processes that microorganisms use to metabolize nickel ions and describes nickel-dependent enzymatic transformations. A wide variety of microbial species sense and respond to nickel ion concentrations by synthesizing nickel-specific transcription factors, and a few possess nickel-responsive riboswitches. During nickel deficiency, some microbes are capable of taking up this micronutrient using influx systems that include ATP binding cassette transporters and secondary transporters such as permeases. Certain microorganisms eliminate excess concentrations of internal nickel ions by using nickel-specific cation diffusion facilitators, major facilitator protein superfamily members, P-type ATPases, and other efflux systems. The basis of nickel toxicity and several mechanisms of nickel resistance also are described in this chapter. Many microorganisms utilize nickel, variously incorporating it into glyoxalase I, acireductone dioxygenase, quercetin 2,4-dioxygenase, superoxide dismutase, urease, [NiFe] hydrogenase, carbon monoxide dehydrogenase, the acetyl-coenzyme A synthase/decarbonylase complex, 2-hydroxyacid racemases and epimerases, and methyl-S-coenzyme M reductase. Auxiliary proteins often function during the biosynthesis of nickel enzymes by delivering the nickel ion, synthesizing a nickel-containing organometallic cofactor, coupling the energy of nucleotide hydrolysis to the metal incorporation, or acting in other ways. Nickel storage proteins are present in some microorganisms. In sum, the microbial metabolism of nickel involves a rich landscape of biological processes.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abreu IA, Cabelli DE (2010) Superoxide dismutases--a review of the metal-associated mechanistic variations. Biochim Biophys Acta 1804:263–274
Adams MWW, Mortenson LE, Chen J-S (1981) Hydrogenase. Biochim Biophys Acta 594:105–176
Addy C, Ohara M, Kawai F, Kidera A, Ikeguchi M, Fuchigami S, Osawa M, Shimada I, Park S-Y, Tame JRH, Heddle JG (2007) Nickel binding to NikA: an additional binding site reconciles spectroscopy, calorimetry and crystallography. Acta Crystallogr D63:221–229
Ahn B-E, Cha J, Lee E-J, Han A-R, Thompson CJ, Roe J-H (2006) Nur, a nickel-responsive regulator of the Fur family, regulates superoxide dismutases and nickel transport in Streptomyces coelicolor. Mol Microbiol 59:1848–1858
Albareda M, Rodrigue A, Brito B, Ruiz-Argüeso T, Imperial J, Mandrand-Berthelot M-A, Palacios J (2015) Rhizobium leguminosarum HupE is a highly-specific diffusion facilitator for nickel uptake. Metallomics 7:691–701
Alfano M, Cavazza C (2020) Structure, function, and biosynthesis of nickel-dependent enzymes. Protein Sci 29:1071–1089
Alfano M, Pérard J, Miras R, Catty P, Cavazza C (2018) Biophysical and structural characterization of the putative nickel chaperone CooT from Carboxydothermus hydrogenoformans. J Biol Inorg Chem 23:809–817
Alfano M, Pérard J, Carpentier P, Basset C, Zambelli B, Timm J, Crouzy S, Ciurli S, Cavazza C (2019a) The carbon monoxide dehydrogenase accessory protein CooJ is a histidine-rich multidomain dimer containing an unexpected Ni(II)-binding site. J Biol Chem 294:7601–7614
Alfano M, Pérard J, Cavazza C (2019b) Nickel-induced oligomerization of the histidine-rich metallochaperone CooJ from Rhodospirillus rubrum. Inorganics 7:84
Alfano M, Veronesi G, Musiani F, Zambelli B, Signor L, Proux O, Rovezzi M, Ciurli S, Cavazza C (2019c) A solvent-exposed cysteine forms a peculiar NiII-binding site in the metallochaperone CooT from Rhodospirillum rubrum. Chem Eur J 25:15351–15360
Allan CB, Wu L-F, Gu Z, Choudhury SB, Al-Mjeni F, Sharma ML, Mandrand-Berthelot M-A, Maroney MJ (1998) An X-ray absorption spectroscopic structural investigation of the nickel site in Escherichia coli NikA protein. Inorg Chem 37:5952–5955
Allen KD, Wegener G, White RH (2014) Discovery of multiple modified F430 coenzymes in methanogens and anaerobic methanotrophic archaea suggests possible new roles for F430 in nature. Appl Environ Microbiol 80:6403–6412
Al-Mjeni F, Ju T, Pochapsky TC, Maroney MJ (2002) XAS investigation of the structure and function of Ni in acireductone dioxygenase. Biochemistry 41:6761–6769
An YJ, Ahn B-E, Han A-R, Kim H-M, Chung KM, Shin J-H, Cho Y-B, Roe J-H, Cha S-S (2009) Structural basis for the specialization of Nur, a nickel-specific Fur homolog, in metal sensing and DNA recognition. Nucleic Acids Res 37:3442–3451
Arima J, Iwabuchi M, Hatanaka T (2004) Gene cloning and overproduction of an aminopeptidase from Streptomyces septatus TH-2, and comparison with a calcium-activated enzyme from Streptomyces griseus. Biochem Biophys Res Commun 317:531–538
Ariza A, Vickers TJ, Greig N, Armour KA, Dixon MJ, Eggleston IM, Fairlamb AH, Bond CS (2006) Specificity of the trypanothione-dependent Leishmania major glyoxalase I: structure and biochemical comparison with the human enzyme. Mol Microbiol 59:1239–1248
Ash PA, Kendall-Price SET, Vincent KA (2019) Unifying activity, structure, and spectroscopy of [NiFe] hydrogenases: combining techniques to clarify mechanistic understanding. Acc Chem Res 52:3120–3131
Atherton JC (2006) The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol 1:63–96
Babich H, Stotzky G (1983) Toxicity of nickel to microbes: environmental aspects. Adv Appl Microbiol 29:195–265
Balasubramanian A, Ponnuraj K (2010) Crystal structure of the first plant urease from jack bean: 83 years of journey from its first crystal to molecular structure. J Mol Biol 400:274–283
Banaszak K, Martin-Diaconescu V, Bellucci M, Zambelli B, Rypniewski W, Maroney MJ, Ciurli S (2012) Crystallographic and x-ray absorption spectroscopic characterization of Helicobacter pylori UreE bound to Ni2+ and Zn2+ reveal a role for the disordered C-terminal arm in metal trafficking. Biochem J 441:1017–1026
Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384
Barondeau DP, Kassman CJ, Bruns CK, Tainer JA, Getzoff ED (2004) Nickel superoxide dismutase structure and mechanism. Biochemistry 43:8038–8047
Bartha R, Ordal EJ (1965) Nickel-dependent chemolithotrophic growth of two Hydrogenomonas strains. J Bacteriol 89:1015–1019
Beaton SE, Evans RM, Finney AJ, Lamont CM, Armstrong FA, Sargent F, Carr SB (2018) The structure of hydrogenase-2 from Escherichia coli: implications for H2-driven proton pumping. Biochem J 475:1353–1370
Becker A, Schlichtling I, Kabsch W, Schultz S, Wagner AFV (1998) Structure of peptide deformylase and identification of the substrate binding site. J Biol Chem 273:11413–11416
Bellucci M, Zambelli B, Musiani F, Turano P, Ciurli S (2009) Helicobacter pylori UreE, a urease accessory protein: specific Ni2+- and Zn2+-binding properties and interaction with its cognate UreG. Biochem J 422:91–100
Benanti EL, Chivers PT (2010) Geobacter uraniireducens NikR displays a DNA binding mode distinct from other members of the NikR family. J Bacteriol 192:4327–4336
Beniamino Y, Pesce G, Zannoni A, Roncarati D, Zambelli B (2020) SrnR from Streptomyces griseus is a nickel-binding transcriptional activator. J Biol Inorg Chem 25:187–198
Benini S, Rypniewski WR, Wilson KS, Miletti S, Ciurli S, Mangani S (1999) A new proposal for urease mechanism based on the crystal structures of the native and inhibited enzyme from Bacillus pasteurii: why urea hydrolysis costs two nickels. Structure 7:205–216
Benini S, Cianci M, Ciurli S (2011) Holo-Ni2+ Helicobacter pylori NikR contains four square-planar nickel-binding sites at physiological pH. Dalton Trans 40:7831–7833
Benoit SL, Maier RJ (2011) Mua (HP0868) is a nickel-binding protein that modulates urease activity in Helicobacter pylori. mBio 2:1–9
Benoit SL, Mehta N, Weinberg MV, Maier C, Maier RJ (2007) Interaction between the Helicobacter pylori accessory proteins HypA and UreE is needed for urease maturation. Microbiology 153:1474–1482
Benoit SL, McMurry JL, Hill SA, Maier RJ (2012) Helicobacter pylori hydrogenase accessory protein HypA and urease accessory protein UreG compete with each other for UreE recognition. Biochim Biophys Acta 1820:1519–1525
Benoit SL, Seshadri S, Lamichhane-Khadka R, Maier RJ (2013) Helicobacter hepaticus NikR controls urease and hydrogenase activities via the NikABDE and HH0418 putative nickel import proteins. Microbiology 159:136–146
Benvenuti M, Meneghello M, Guendon C, Jacq-Bailly A, Jeoung J-H, Dobbek H, Léger C, Fourmond V, Dementin S (2020) The two CO-dehydrogenases of Thermococcus sp. AM4. Biochim Biophys Acta 1861:148188
Beveridge TJ, Murray RGE (1976) Uptake and retention of metals by cell walls of Bacillus subtilis. J Bacteriol 127:1502–1518
Bienert GP, Desguin B, Chaumont F, Hols P (2013) Channel-mediated lactic acid transport: a novel function for aquaglyceroporins in bacteria. Biochem J 454:559–570
Blahut M, Dzul S, Wang S, Kandegedara A, Grossoehme NE, Stemmler TL, Outten FW (2018) Conserved cysteine residues are necessary for nickel-induced allosteric regulation of the metalloregulatory protein YqjI (NfeR) in E. coli. J Inorg Biochem 194:123–133
Blériot C, Effantin G, Lagarde F, Mandrand-Berthelot M-A, Rodrique A (2011) RcnB is a periplasmic protein essential for maintaining intracellular Ni and Co concentrations in Escherichia coli. J Bacteriol 193:3785–3793
Blériot C, Gault M, Gueguen E, Arnoux P, Mandrand-Berthelot M-A, Rodrigue A (2015) Cu binding by the Escherichia coli metal-efflux accessory protein RcnB. Metallomics 6:1400–1409
Blokesch M, Rohrmoser M, Rode S, Böck A (2004) HybF, a zinc-containing protein involved in NiFe hydrogenase biosynthesis. J Bacteriol 186:2603–2611
Bloom SB, Zamble DB (2004) Metal-selective DNA-binding response of Escherichia coli NikR. Biochemistry 43:10029–10038
Bobik TA, Olson KD, Noll KN, Wolfe RS (1987) Evidence that the heterodisulfide of coenzyme M and 7-mercaptoheptanoylthreonine phosphate is a product of the methylreductase reaction in Methanobacterium. Biochem Biophys Res Commun 149:455–460
Böck A, King PW, Blokesch M, Posewitz MC (2006) Maturation of hydrogenases. Adv Microb Physiol 51:1–71
Boer JL, Quiroz-Valenzuela S, Anderson KL, Hausinger RP (2010) Mutagenesis of Klebsiella aerogenes UreG to probe nickel binding and interactions with other urease-related proteins. Biochemistry 49:5859–5869
Boer JL, Mulrooney SB, Hausinger RP (2014) Nickel-dependent metalloenzymes. Arch Biochem Biophys 544C:142–152
Bonacker LG, Baudner S, Mörschel E, Böcher R, Thauer RK (1993) Properties of the two isoenzymes of methyl-coenzyme M reductase in Methanobacterium thermoautotrophicum. Eur J Biochem 217:587–595
Bonam D, Ludden PW (1987) Purification and characterization of carbon monoxide dehydrogenase, a nickel, zinc, iron-sulfur protein, from Rhodospirillum rubrum. J Biol Chem 262:2980–2987
Bonam D, McKenna MC, Stephens PJ, Ludden PW (1988) Nickel-deficient carbon monoxide dehydrogenase from Rhodospirillum rubrum: in vivo and in vitro activation by exogenous nickel. Proc Natl Acad Sci U S A 85:31–35
Bossè JT, Gilmour HD, MacInnes JI (2001) Novel genes affecting urease activity in Actinobacillus pleuropneumoniae. J Bacteriol 183:1242–1247
Brauer AL, Learman BS, Armbruster CE (2020) Ynt is the primary nickel import system used by Proteus mirabilis and specifically contributes to fitness by supplying nickel for urease activity. Mol Microbiol 114:185–199
Braun V, Hantke K (2011) Recent insights into iron import by bacteria. Curr Opin Chem Biol 15:328–334
Brito B, Prieto R-I, Cabrera E, Mandrand-Berthelot M-A, Imperial J, Ruiz-Argüeso T, Palacios J-M (2010) Rhizobium leguminosarum hupE encodes a nickel transporter required for hydrogenase activity. J Bacteriol 192:925–935
Bryngelson PA, Arobo SE, Pinkham JL, Cabelli DE, Maroney MJ (2004) Expression, reconstitution, and mutation of recombinant Streptomyces coelicolor NiSOD. J Am Chem Soc 126:460–461
Buan NR, Escalante-Semerena JC (2006) Purification and initial biochemical characterization of ATP: cob(I)alamin adenosyltransferase (EutT) enzyme of salmonella enterica. J Biol Chem 281:16971–16977
Budnick JA, Prado-Sanchez E, Caswell CC (2018) Defining the regulatory mechanism of NikR, a nickel-responsive transcription regulator, in Brucella abortus. Microbiology 164:1320–1325
Burne RA, Chen Y-YM (2000) Bacterial ureases in infectious diseases. Microbes Infect 2:533–542
Bury-Moné S, Thiberg J-M, Contreras M, Maitournam A, Labigne A, De Reuse H (2004) Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori. Mol Microbiol 53:623–638
Busenlehner LS, Pennella MA, Giedroc DP (2003) The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance. FEMS Microbiol Rev 27:131–143
Campbell DR, Chapman KE, Waldron KJ, Tottey S, Kendall S, Cavallaro G, Andreini C, Hinds J, Stoker NG, Robinson NJ, Cavet JS (2007) Mycobacterial cells have dual nickel-cobalt sensors. Sequence relationships and metal sites of metal-responsive repressors are not congruent. J Biol Chem 282:32298–32310
Campeciño JO, Maroney MJ (2017) Reinventing the wheel: the NiSOD story. In: Zamble D, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. The Royal Society for Chemistry, Cambridge
Camporesi G, Minzoni A, Morasso L, Ciurli S, Musiani F (2021) Nickel import and export in the human pathogen Helicobacter pylori, perspectives from molecular modelling. Metallomics 13(12):mfab066. https://doi.org/10.1093/mtomcs/mfab066
Can M, Armstrong FA, Ragsdale SW (2014) Structure, function, and mechanism of the nickel metalloenzymes, CO dehydrogenase, and acetyl-CoA synthase. Chem Rev 114:4149–4174
Carr CE, Foster AW, Maroney MJ (2017a) An XAS investigation of the nickel site structure in the transcriptional regulator InrS. J Inorg Biochem 177:352–358
Carr CE, Musiani F, Huang H-T, Chivers PT, Ciurli S, Maroney MJ (2017b) Glutamate ligation in the Ni(II)- and Co(II)-responsive Escherichia coli transcriptional regulator, RcnR. Inorg Chem 56:6459–6476
Carter EL, Hausinger RP (2010) Characterization of Klebsiella aerogenes urease accessory protein UreD in fusion with the maltose binding protein. J Bacteriol 192:2294–2304
Carter EL, Tronrud DE, Taber SR, Karplus PA, Hausinger RP (2011) Iron-containing urease in a pathogenic bacterium. Proc Natl Acad Sci U S A 108:13095–13099
Cavet JS, Meng W, Pennella MA, Appelhoff RJ, Giedroc DP, Robinson NJ (2002) A nickel-cobalt sensing ArsR-SmtB family repressor: contributions of cytosol and effector binding sites to metal selectivity. J Biol Chem 277:38441–38448
Chai SC, Ju T, Dang M, Goldsmith RB, Maroney MJ, Pochapsky TC (2008) Characterization of metal binding in the active sites of acireductone dioxygenase isoforms from Klebsiella ATCC 8724. Biochemistry 47:2428–2438
Chaintreuil C, Rigault F, Moulin L, Jaffré T, Fardoux J, Giraud E, Dreyfus B, Bailly X (2007) Nickel resistance determinants in Bradyrhizobium strains from nodules of the endemic New Caledonia legume Serianthes calycina. Appl Environ Microbiol 73:8018–8022
Chang Z, Kuchar J, Hausinger RP (2004) Chemical crosslinking and mass spectrometric identification of sites of interaction for UreD, UreF, and urease. J Biol Chem 279:15305–15313
Chapot-Chartier M-P, Kulakauskas S (2014) Cell wall structure and function in lactic acid bacteria. Microb Cell Factories 13(Suppl 1):59
Chen Y-YM, Burne RA (2003) Identification and characterization of the nickel uptake system for urease biosynthesis in Streptococcus salivarius 57.I. J Bacteriol 185:6773–6779
Chen YP, Dilworth MJ, Glenn AR (1984) Aromatic metabolism in Rhizobium trifolii - protocatechuate 3,4-dioxygenase. Arch Microbiol 138:187–190
Chen YP, Glenn AR, Dilworth MJ (1985) Aromatic metabolism in Rhizobium trifolii - catechol 1,2-dioxygenase. Arch Microbiol 141:225–228
Chen S-C, Musat N, Lechtenfeld OJ, Paschke H, Schmidt M, Said N, Popp D, Calabrese F, Stryhanyuk H, Jaekel U, Zhu Y-G, Joye SB, Richnow H-H, Widdel F, Musat F (2019) Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep. Nature 568:108–111
Chen H, Gan Q, Fan C (2020) Methyl-coenzyme M reductase and its post-translational modifications. Front Microbiol 11:578356
Cheng Z, Wei YYC, Sung WWL, Glick BR, McConkey BJ (2009) Proteomic analysis of the response of the plant growth-promoting bacterium Pseudomonas putida UW4 to nickel stress. Proteome Sci 7:18
Cheng T, Li H, Xia W, Jin L, Sun H (2016) Exploration into the nickel ‘microcosmos’ in prokaryotes. Coord Chem Rev 311:24–37
Cherrier MV, Martin L, Cavazza C, Jacquamet L, Lemaire D, Gaillard J, Fontecilla-Camps JC (2005) Crystallographic and spectroscopic evidence for high affinity binding of FeEDTA(H2O)− to the periplasmic nickel transporter NikA. J Am Chem Soc 127:10075–10082
Cherrier MV, Cavazza C, Bochot C, Lemaire D, Fontecilla-Camps JC (2008) Structural characterization of a putative endogenous metal chelator in the periplasmic nickel transporter NikA. Biochemistry 47:9937–9943
Chivers PT (2015) Nickel recognition by bacterial importer proteins. Metallomics 7:590–595
Chivers PT (2017) Nickel regulation. In: Zamble DB, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. Royal Society of Chemistry, Cambridge
Chivers PT, Sauer RT (2000) Regulation of high affinity nickel uptake in bacteria. Ni2+-dependent interaction of NikR with wild-type and mutant operator sites. J Biol Chem 275:19735–19741
Chivers PT, Sauer RT (2002) NikR repressor: high-affinity nickel binding to the C-terminal domain regulates binding to operator DNA. Chem Biol 9:1141–1148
Chivers PT, Tahirov TH (2005) Structure of Pyrococcus horikoshi NikR: nickel sensing and implications for the regulation of DNA recognition. J Mol Biol 348:597–607
Chivers PT, Benanti EL, Heil-Chapdelaine V, Iwig JS, Rowe JL (2012) Identification of Ni-(L-His)2 as the substrate for NikABCDE-dependent nickel uptake in Escherichia coli. Metallomics 4:1043–1050
Choudhury SB, Lee J-W, Davidson G, Yim Y-I, Bose K, Sharma ML, Kang S-O, Cabelli DE, Maroney MJ (1999) Examination of the nickel site structure and reaction mechanism in Streptomyces seoulensis superoxide dismutase. Biochemistry 38:3744–3752
Chung H-Y, Choi J-H, Kim E-J, Cho Y-H, Roe J-H (1999) Negative regulation of the gene for Fe-containing superoxide dismutase by an Ni-responsive factor in Streptomyces coelicolor. J Bacteriol 181:7381–7384
Clugston SL, Barnard JFJ, Kinach R, Miedema D, Ruman R, Daub E, Honek JF (1998) Overproduction and characterization of a dimeric non-zinc glyoxylase I from Escherichia coli: evidence for optimal activation by nickel ions. Biochemistry 37:8754–8763
Cohen SE, Brignole EJ, Wittenborn EC, Can M, Thompson S, Ragsdale SW, Drennan CL (2020) Negative-stain electron microscopy reveals dramatic structural rearrangements in Ni-Fe-S-dependent carbon monoxide dehydrogenase/acetyl-CoA synthase. Structure 28:1–7
Collins CM, D’Orazio SEF (1993) Bacterial ureases: structure, regulation of expression and role in pathogenesis. Mol Microbiol 9:907–913
Colpas GJ, Hausinger RP (2000) In vivo and in vitro kinetics of metal transfer by the Klebsiella aerogenes urease nickel metallochaperone, UreE. J Biol Chem 275:10731–10737
Colpas GJ, Brayman TG, McCracken J, Pressler MA, Babcock GT, Ming L-J, Colangelo CM, Scott RA, Hausinger RP (1998) Spectroscopic characterization of metal binding by Klebsiella aerogenes UreE urease accessory protein. J Biol Inorg Chem 3:150–160
Colpas GJ, Brayman TG, Ming L-J, Hausinger RP (1999) Identification of metal-binding residues in the Klebsiella aerogenes urease nickel metallochaperone, UreE. Biochemistry 38:4078–4088
Constant P, Chowdhury SP, Pratscher J, Conrad R (2010) Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase. Environ Microbiol 12:821–829
Constant P, Chowdhury SP, Hesse L, Pratscher J, Conrad R (2011) Genome data mining and soil survey for the novel group 5 [NiFe]-hydrogenase to explore the diversity and ecological importance of presumptive high-affinity H2-oxidizing bacteria. Appl Environ Microbiol 77:6027–6035
Contreras M, Thiberge J-M, Mandrand-Berthelot M-A, Labigne A (2003) Characterization of the roles of NikR, a nickel-responsive pleiotropic autoregulator of Helicobacter pylori. Mol Microbiol 49:947–963
Covacci A, Telford JL, Del Giudice G, Parsonet J, Rappuoli R (1999) Helicobacter pylori virulence and genetic geography. Science 284:1328–1333
Cubillas C, Vinuesa P, Tabche ML, Garcia-de los Santos A (2013) Phylogenomic analysis of cation diffusion facilitator proteins uncovers Ni2+/Co2+ transporters. Metallomics 5:1634–1643
Cunha ES, Chen X, Sanz-Gaitero M, Mills DJ, Luecke H (2021) Cryo-EM structure of helicobacter pylori urease with an inhibitor in the active site at 2.0 Å resolution. Nat Commun 12:230
Cussac V, Ferrero RL, Labigne A (1992) Expression of Helicobacter pylori urease genes in Escherichia coli grown under nitrogen-limiting conditions. J Bacteriol 174:2466–2473
Cvetkovic A, Menon AL, Thorgersen MP, Scott JW, Poole FL II, Jenney FE Jr, Lancaster WA, Praissman JA, Shanmukh S, Vaccaro BJ, Trauger SA, Kalisiak E, Apon JV, Siuzdak G, Yannone SM, Tainer JA, Adams MWW (2010) Microbial metalloproteomes are largely uncharacterized. Nature 466:779–782
Dai Y, Wensink PC, Abeles RH (1999) One protein, two enzymes. J Biol Chem 274:1193–1195
Darnault C, Volbeda A, Kim EJ, Legrand P, Vernède X, Lindahl PA, Fontecilla-Camps JC (2003) NiZn[Fe4S4] and NiNi[Fe4S4] clusters in closed and open a subunits of acetyl-CoA synthase/carbon monoxide dehydrogenase. Nat Struct Mol Biol 10:271–279
Darrouzet E, Rinaldi C, Zambelli B, Ciurli S, Cavazza C (2021) Revisiting the CooJ family, a potential chaperone for nickel delivery to [NiFe]-carbon monoxide dehydrogenase. J Inorg Biochem 225:111588. https://doi.org/10.1016/j.jinorgbio.2021.111588
Davidson G, Clugston SL, Honek JF, Maroney MJ (2000) XAS investigation of the nickel active site structure in Escherichia coli glyoxalase I. Inorg Chem 39:2962–2963
Davidson G, Clugston SL, Honek JF, Maroney MJ (2001) An XAS investigation of product and inhibitor complexes of Ni-containing GlxI from Escherichia coli: mechanistic implications. Biochemistry 40:4569–4582
Davis GS, Flannery EL, Mobley HLT (2006) Helicobacter pylori HP1512 is a nickel-responsive NikR-regulated outer membrane protein. Infect Immun 74:6811–6820
de Pina K, Navarro C, McWalter L, Boxer DH, Price NC, Kelly SM, Mandrand-Berthelot M-A, Wu L-F (1995) Purification and characterization of the periplasmic nickel-binding protein NikA of Escherichia coli K12. Eur J Biochem 227:857–865
de Pina K, Desjardin V, Mandrand-Berthelot M-A, Giordano G, Wu L-F (1999) Isolation and characterization of the nikR gene encoding a nickel-responsive regulator in Escherichia coli. J Bacteriol 181:670–674
Debussche L, Couder M, Thibaut D, Cameron B, Crouzet J, Blanche F (1992) Assay, purification, and characterization of cobaltochelatase, a unique complex catalyzing cobalt insertion in hydrogenobyrinic acid a,c-diamide during coenzyme B12 biosynthesis in Pseudomonas denitrificans. J Bacteriol 174:7445–7451
Degen O, Kobayashi M, Shimizu S, Eitinger T (1999) Selective transport of divalent cations by transition metal permeases: the Alcaligenes eutrophus HoxN and the Rhodococcus rhodochrous NhlF. Arch Microbiol 171:139–145
Delany I, Ieva R, Soragni A, Hilleringmann M, Rappuoli R, Scarlato V (2005) In vitro analysis of protein-operator interactions of the NikR and Fur metal-responsive regulators of coregulated genes in Helicobacter pylori. J Bacteriol 187:7703–7715
Denic M, Turlin E, Michel V, Fischer F, Khorasani-Motlagh M, Zamble D, Vinella D, de Reuse H (2021) A novel mode of control of nickel uptake by a multifunctional metallochaperone. PLoS Pathog 17:e1009193
Desguin B, Goffin P, Viaene E, Kleerebezem M, Martin-Diaconescu V, Maroney MJ, Declercq J-P, Soumillion P, Hols P (2014) Lactate racemase is a nickel-dependent enzyme activated by a widespread maturation system. Nat Commun 5:3615
Desguin B, Goffin P, Bakouche N, Diman A, Viaene E, Dandoy D, Fontaine L, Hallet B, Hols P (2015a) Enantioselective regulation of lactate racemization by LarR in Lactobacillus plantarum. J Bacteriol 197:219–330
Desguin B, Zhang T, Soumillion P, Hols P, Hu J, Hausinger RP (2015b) A tethered niacin-derived pincer complex with a nickel-carbon bond in lactate racemase. Science 349:66–69
Desguin B, Soumillion P, Hols P, Hausinger RP (2016) Nickel-pincer cofactor biosynthesis involves LarB-catalyzed pyridinium carboxylation and LarE-dependent sacrificial sulfur insertion. Proc Natl Acad Sci U S A 113:5598–5603
Desguin B, Soumillion P, Hols P, Hu J, Hausinger RP (2017) Lactate racemase and its niacin-derived, covalently-tethered, nickel cofactor. In: Zamble DB, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. Royal Society of Chemistry, Cambridge
Desguin B, Fellner M, Riant O, Hu J, Hausinger RP, Hols P, Soumillion P (2018) Biosynthesis of the nickel-pincer nucleotide cofactor of lactate racemase requires a CTP-dependent cyclometallase. J Biol Chem 293:12303–12317
Desguin B, Urdiain-Arraiza J, Da Costa M, Fellner M, Hu J, Hausinger RP, Desmet T, Hols P, Soumillion P (2020) Uncovering a superfamily of nickel-dependent hydroxyacid racemases and epimerases. Sci Rep 10:18123
Deshpande A, Pochapsky TC, Ringe D (2017) The metal drives the chemistry: dual functions of acireductone dioxygenase. Chem Rev 117:10474–10501
Dian C, Schauer K, Kapp U, McSweeney SM, Labigne A, Terradot L (2006) Structural basis of the nickel response in Helicobacter pylori: crystal structures of HpNikR in apo and nickel-bound states. J Mol Biol 361:715–730
Diederix REM, Fauquant C, Rodrigue A, Mandrand-Berthelot M-A, Michaud-Soret I (2008) Sub-micromolar affinity of Escherichia coli NikR for Ni(II). Chem Commun 1813–1815
Dixon NE, Gazzola C, Blakeley RL, Zerner B (1975) Jack bean urease (EC 3.5.1.5). A metalloenzyme. A simple biological role for nickel? J Am Chem Soc 97:4131–4133
Dobbek H, Svetlitchnyi V, Gremer L, Huber R, Meyer O (2001) Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science 293:1281–1285
Dokpikul T, Chaoprasid P, Saninjuk K, Sirirakphaisarn S, Johnrod J, Nookabkaew S, Sukchawilit R, Mongkolsuk S (2016) Regulation of the cobalt/nickel efflux operon dmeRF in Agrobacterium tumefaciens and a link between the iron-sensing regulator RirA and cobalt/nickel resistance. Appl Environ Microbiol 82:4732–4742
Domnik L, Merrouch M, Goetzl S, Jeoung J-H, Léger C, Dementin S, Fourmond V, Dobbek H (2017) CODH-IV: a high-efficiency CO-scavenging CO dehydrogenase with resistance to O2. Angew Chem Int Ed 56:15466–15469
Dosanjh NS, West AL, Michel SL (2009) Helicobacter pylori NikR’s interaction with DNA: a two-tiered mode of recognition. Biochemistry 48:527–536
Doukov TI, Iverson TM, Seravalli J, Ragsdale SW, Drennan CL (2002) A Ni-Fe-Cu center in a bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase. Science 298:567–272
Doukov TI, Blasiak LC, Seravalli J, Ragsdale SW, Drennan CL (2008) Xenon in and at the end of the tunnel of bifunctional carbon monoxide dehydrogenase/acetyl-CoA synthase. Biochemistry 47:3474–3483
Drennan CL, Heo J, Sintchak MD, Schreiter E, Ludden PW (2001) Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni-Fe-S carbon monoxide dehydrogenase. Proc Natl Acad Sci U S A 98:11973–11978
Dupont CL, Neupane K, Shearer J, Palenik B (2008) Diversity, function and evolution of genes coding for putative Ni-containing superoxide dismutases. Environ Microbiol 10:1831–1843
Dupont CL, Johnson DA, Phillippy K, Paulsen IT, Brahamsha B, Palenik B (2012) Genetic identification of a high-affinity Ni transporter and the transcriptional response to Ni deprivation in Synechococcus sp. strain WH8102. Appl Environ Microbiol 78:7822–7832
D’Urzo A, Santambrogio C, Grandori R, Ciurli S, Zambelli B (2014) The conformational response to Zn(II) and Ni(II) binding of Sporosarcina pasteurii UreG, an intrinsically disordered GTPase. J Biol Inorg Chem 19:1341–1354
Eberz G, Eitinger T, Friedrich B (1989) Genetic determinants of a nickel-specific transport system are part of the plasmid-encoded hydrogenase gene cluster in Alcaligenes eutrophus. J Bacteriol 171:1340–1345
Eitinger T (2004) In vivo production of active nickel superoxide dismutase from Prochlorococcus marinus MIT9313 is dependent on its cognate peptidase. J Bacteriol 186:7812–7825
Eitinger T, Friedrich B (1991) Cloning, nucleotide sequence, and heterologous expression of the high-affinity nickel transport gene from Alcaligenes eutrophus. J Biol Chem 266:3222–3227
Eitinger T, Friedrich B (1994) A topological model for the high-affinity nickel transporter of Alcaligenes eutrophus. Mol Microbiol 12:1025–1032
Eitinger T, Mandrand-Berthelot M-A (2000) Nickel transport systems in microorganisms. Arch Microbiol 173:1–9
Eitinger T, Wolfram L, Degen O, Anthon C (1997) A Ni2+ binding motif is the basis of high affinity transport of the Alcaligenes eutrophus nickel permease. J Biol Chem 272:17139–17144
Eitinger T, Degen O, Böhnke U, Müller M (2000) Nic1p, a relative of bacterial transition metal permeases in Schizosaccharomyces pombe, provides nickel ion for urease biosynthesis. J Biol Chem 275:18029–18033
Eitinger T, Suhr J, Moore L, Smith JAC (2005) Secondary transporters for nickel and cobalt ions: theme and variations. Biometals 18:399–405
Ellefson WL, Wolfe RS (1981) Component C of the methylreductase system of Methanobacterium. J Biol Chem 256:4259–4262
Ellefson WL, Whitman WB, Wolfe RS (1982) Nickel-containing factor F430: chromophore of the methylreductase of Methanobacterium. Proc Natl Acad Sci U S A 79:3707–3710
Ellermann J, Hedderich R, Böcher R, Thauer RK (1988) The final step in methane formation. Investigations with the highly purified methyl-CoM reductase (component C) from Methanobacterium thermoautotrophicum (strain Marburg). Eur J Biochem 172:669–677
Englert DL, Adase CA, Jayaraman A, Manson MD (2010) Repellent taxis in response to nickel ion requires neither Ni2+ transport nor the periplasmic NikA binding protein. J Bacteriol 192:2633–2637
Ensign SA, Campbell MJ, Ludden PW (1990) Activation of the nickel-deficient carbon monoxide dehydrogenase from Rhodospirillum rubrum: kinetic characterization and reductant requirement. Biochemistry 29:2162–2168
Ermler U, Grabarse W, Shima S, Goubeaud M, Thauer RK (1997) Crystal structure of methyl-coenzyme M reductase: the key enzyme of biological methane formation. Science 278:1457–1462
Ernst FD, Kuipers EJ, Heijens A, Sarwari R, Stoof J, Penn CW, Kusters JG, van Vliet AH (2005) The nickel-responsive regulator NikR controls activation and repression of gene transcription in Helicobacter pylori. Infect Immun 73:7252–7258
Ernst FD, Stoof J, Horrevoets WM, Kuipers EJ, Kusters JG, Van Vliet AHM (2006) NikR mediates nickel-responsive transcriptional repression of the Helicobacter pylori outer membrane proteins FecA3 (HP1400) and FrpB4 (HP1512). Infect Immun 74:6821–6828
Eschweiler JD, Farrugia MA, Hausinger RP, Ruotolo BT (2018) A structural model of the urease activation complex derived from ion mobility-mass spectrometry and integrative modeling. Structure 26:599–606
Farrugia MA, Han L, Zhong Y, Boer JL, Ruotolo BT, Hausinger RP (2013a) Analysis of a soluble (UreD:UreF:UreG)2 accessory protein complex and its interactions with Klebsiella aerogenes urease by mass spectroscopy. J Am Soc Mass Spectrom 24:1328–1337
Farrugia MA, Macomber L, Hausinger RP (2013b) Biosynthesis of the urease metallocenter. J Biol Chem 288:13178–13185
Farrugia MA, Wang B, Feig M, Hausinger RP (2015) Mutational and computational evidence that a nickel-transfer tunnel in UreD is used for activation of Klebsiella aerogenes urease. Biochemistry 54:6392–6401
Fellner M, Desguin B, Hausinger RP, Hu J (2017) Structural insights into the catalytic mechanism of a sacrificial sulfur insertase of the N-type ATP pyrophosphatase family, LarE. Proc Natl Acad Sci U S A 114:9074–9079
Fetzner S (2012) Ring-cleaving dioxygenases with a cupin fold. Appl Environ Microbiol 78:2505–2514
Finkenwirth F, Eitinger T (2019) ECF-type ABC transporters for uptake of vitamins and transition metal ions into prokaryotic cells. Res Microbiol 170:358–365
Fischer F, Robbe-Saule M, Turlin E, Mancuso F, Michel V, Richaud P, Veyrier FJ, De Reuse H, Vinella D (2016) Characterization in Helicobacter pylori of a nickel transporter essential for colonization that was acquired during evolution by gastric Helicobacter species. PLoS Pathog 12:e1006018
Flannigan R, Choi WH, Chew B, Lange D (2014) Renal struvite stones--pathogenesis, microbiology, and management strategies. Nat Rev Urol 11:333–341
Fong YH, Wong HC, Chuck CP, Chen YW, Sun H, Wong K-B (2011) Assembly of the preactivation complex for urease maturation in Helicobacter pylori: crystal structure of the UreF/UreH protein complex. J Biol Chem 286:43241–43249
Fong YH, Wong HC, Yuen MH, Lau PH, Chen YW, Wong K-B (2013) Structure of UreG/UreF/UreH complex reveals how urease accessory proteins facilitate maturation of Helicobacter pylori urease. PLoS Biol 11:e1001678
Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107:4273–4303
Fortin D, Southam G, Beveridge TJ (1994) Nickel sulfide, iron-nickel sulfide and iron sulfide precipitated by a newly isolated Desulfotomaculum species and its relation to nickel resistance. FEMS Microbiol Ecol 14:121–132
Forzi L, Sawers RG (2007) Maturation of [NiFe]-hydrogenases in Escherichia coli. Biometals 20:565–578
Foster AW, Patterson CJ, Pernil R, Hess CR, Robinson NJ (2012) Cytosolic Ni(II) sensor in cyanobacterium. Nickel detection follows nickel affinity across four families of sensors. J Biol Chem 287:12142–12151
Foster AW, Pernil R, Patterson CJ, Robinson NJ (2014) Metal specificity of cyanobacterial nickel-responsive repressor InrS: cells maintain zinc and copper below the detection threshold for InrS. Mol Microbiol 92:797–812
Foster AW, Pernil R, Patterson CJ, Scott AJP, Palsson LO, Pal R, Cummins I, Chivers PT, Pohl E, Robinson NJ (2017) A light tunable range for Ni(II) sensing and buffering in cells. Nat Chem Biol 13:409–414
Fourcroy AF, Vauguelin LN (1799) Extrait d’un premier mémoire des cit. Fourcroy et Vaugueline poru servir a l’histoire naturelle, chemique et médicale de l’urine humanine, contentant quelques faits nouveaux sur son analyse et son altération spontanée. Ann Chim 31:48–71
Fritsche E, Paschos A, Beisel H-G, Böck A, Huber R (1999) Crystal structure of the hydrogenase maturating endopeptidase HydD from Escherichia coli. J Mol Biol 288:989–998
Fu C, Javedan S, Moshiri F, Maier RJ (1994) Bacterial genes involved in incorporation of nickel into a hydrogenase enzyme. Proc Natl Acad Sci U S A 91:5099–5103
Fu C, Olson JW, Maier RJ (1995) HypB protein of Bradyrhizobium japonicum is a metal-binding GTPase capable of binding 18 divalent nickel ions per dimer. Proc Natl Acad Sci U S A 92:2333–2337
Fulkerson JF Jr, Mobley HLT (2000) Membrane topology of the NixA nickel transporter of Helicobacter pylori: two nickel transport-specific motifs within transmembrane helices II and III. J Bacteriol 182:1722–1730
Fulkerson JF Jr, Garner RM, Mobley HLT (1998) Conserved residues and motifs in the NixA protein of Helicobacter pylori are critical for the high affinity transport of nickel ions. J Biol Inorg Chem 273:235–241
Furukawa K, Ramesh A, Zhou Z, Weinberg Z, Vallery T, Winkler WC, Breaker RR (2015) Bacterial riboswitches cooperatively bind Ni2+ or Co2+ ions and control expression of heavy metal transporters. Mol Cell 57:1088–1098
Gadd GM, Griffiths AJ (1978) Microorganisms and heavy metal toxicity. Microb Ecol 4:303–317
Garcia-Dominguez M, Lopez-Maury L, Florencio FJ, Reyes JC (2000) A gene cluster involved in metal homeostasis in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 182:1507–1514
Garcin E, Vernede X, Hatchikian EC, Volbeda A, Frey M, Fontecilla-Camps JC (1999) The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center. Structure 7:557–566
Ge R, Watt RM, Sun X, Tanner JA, He Q-Y, Huang J-D, Sun H (2006a) Expression and characterization of the histidine-rich protein, Hpn: potential for nickel storage in Helicobacter pylori. Biochem J 393:285–293
Ge R, Zhang Y, Sun X, Watt RM, He Q-Y, Huang J-D, Wilcox DE, Sun H (2006b) Thermodynamic and kinetic aspects of metal binding properties of the histidine-rich protein, Hpn. J Am Chem Soc 128:11330–11331
Gencic S, Grahame DA (2003) Nickel in subunit b of the acetyl-CoA decarbonylase/synthase multienzyme complex in methanogens. Catalytic properties and evidence for a binuclear Ni-Ni site. J Biol Chem 278:6101–6110
Geslin C, Llanos J, Prieur D, Jeanthon C (2001) The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res Microbiol 152:901–905
Ghosh S, Sadhukhan PC, Chaudhuri J, Ghosh DK, Mandal A (1999) Purification and properties of mercuric reductase from Azotobacter chroococcum. J Appl Microbiol 86:7–12
Ghssein G, Brutesco C, Ouerdane L, Fojcik C, Izaute A, Wang S, Hajjar C, Lobinski R, Lemaire D, Richaud P, Voulhoux R, Espaillat A, Cava F, Pignol D, Borezée-Durant E, Arnoux P (2016) Biosynthesis of a broad-spectrum nicotianamine-like metallophore in Staphylococcus aureus. Science 352:1105–1109
Gilbert JV, Ramakrishna J, Sunderman FW Jr, Wright A, Plaut AG (1995) Protein Hpn: cloning and characterization of a histidine-rich metal-binding polypeptide in Helicobacter pylori and Helicobacter mustelae. Infect Immun 63:2682–2688
Glass JB, Dupont CL (2017) Oceanic nickel biogeochemistry and the evolution of nickel use. In: Zamble DB, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. Royal Society of Chemistry, Cambridge
Gong W, Hao B, Wei Z, Ferguson DJ Jr, Tallant T, Krzycki JA, Chan MK (2008) Structure of the a2e2 Ni-dependent CO dehydrogenase component of the Methanosarcina barkeri acetyl-CoA decarbonylase/synthase complex. Proc Natl Acad Sci U S A 105:9558–9563
Gourdon P, Liu X-Y, Skjorringe T, Morth JP, Moller LB, Pedersen BP, Nissen P (2011) Crystal structure of a copper-transporting PIB-type ATPase. Nature 475:59–64
Grabarse W, Mahlert F, Shima S, Thauer RK, Ermler U (2000) Comparison of three methyl-coenzyme M reductases from phylogenetically distant microorganisms: unusual amino acid modification, conservation, and adaptation. J Mol Biol 303:329–344
Grahame DA (1991) Catalysis of acetyl-CoA cleavage and tetrahydrosarcinapterin methylation by a carbon monoxide dehydrogenase-corrinoid enzyme complex. J Biol Chem 266:22227–22233
Grass G, Grobe C, Nies D (2000) Regulation of the cnr cobalt and nickel resistance determinant from Ralstonia sp. strain CH34. J Bacteriol 182:1390–1398
Grass G, Fan B, Rosen BP, Lemke K, Schlegel HG, Rensing C (2001) NreB from Achromobacter xylosoxidans 31A is a nickel-induced transporter conferring nickel resistance. J Bacteriol 183:2803–2807
Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, Cook GM, Morales SE (2016) Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilized energy source for microbial growth and survival. ISME J 10:761–777
Gregg CM, Goetzl S, Jeong J-H, Dobbek H (2016) AcsF catalyzes the ATP-dependent insertion of nickel into the Ni,Ni-[4Fe4S] cluster of acetyl-CoA synthase. J Biol Chem 291:18129–18138
Greig N, Wyllie S, Vickers TJ, Fairlamb AH (2006) Trypanothione-dependent glyoxalase I in Trypanosoma cruzi. Biochem J 400:217–223
Griffith DP, Musher DM, Itin C (1976) Urease. The primary cause of infection-induced urinary stones. Investig Urol 13:346–350
Grossoehme NE, Mulrooney SB, Hausinger RP, Wilcox DE (2007) Thermodynamics of Ni2+, Cu2+, and Zn2+ binding to urease metallochaperone UreE. Biochemistry 46:10506–10516
Guldan H, Sterner R, Babinger P (2008) Identification and characterization of a bacterial glycerol-1-phosphate dehydrogenase: Ni2+-dependent AraM from Bacillus subtilis. Biochemistry 47:7376–7384
Guo H, Liu H, Wu H, Cui H, Fang J, Zuo Z, Deng J, Li Y, Wang X, Zhao L (2019) Nickel carcinogenesis mechanism: DNA damage. Int J Mol Sci 20:4690
Ha N-C, Oh S-T, Sung JY, Cha KA, Lee MH, Oh B-H (2001) Supramolecular assembly and acid resistance of Helicobacter pylori urease. Nat Struct Biol 8:505–509
Hadj-Saïd J, Pandelia M-E, Léger C, Fourmond V, Dementin S (2015) The carbon monoxide dehydrogenase from Desulfovibrio vulgaris. Biochim Biophys Acta 1847:1574–1583
Hahn CJ, Laso-Pérez R, Vulcano F, Vaziourakis K-M, Stokke R, Steen IH, Teske A, Boetius A, Liebeke M, Amann R, Knittel K, Wegener G (2020) “Candidatus Ethanoperedens,” a thermophilic genus of archaea mediating the anaerobic oxidation of ethane. mBio 11:e00600–e00620
Hahn CJ, Lemaire ON, Kahnt J, Engilberge S, Wegener G, Wagner T (2021) Crystal structure of a key enzyme for anaerobic ethane activation. Science 373(6550):118–121. https://doi.org/10.1126/science.abg1765
Hall DR, Leonard GA, Reed CD, Watt CI, Berry A, Hunter WN (1999) The crystal structure of Escherichia coli class II fructose-1, 6-bisphosphate aldolase in complex with phosphoglycolohydroxamate reveals details of mechanism and specificity. J Mol Biol 287:383–394
Happe RP, Roseboom W, Pierik AJ, Albracht SPJ, Bagley KA (1997) Biological activation of hydrogen. Nature 385:126
Haritha A, Sagar KP, Tiwari A, Kiranmavi P, Rodrigue A, Mohan PM, Singh SS (2009) MrdH, a novel metal resistance determinant of Pseudomonas putida KT 2440, is flanked by metal-inducible mobile genetic elements. J Bacteriol 191:5976–5987
Hausinger RP, Orme-Johnson WH, Walsh C (1984) Nickel tetrapyrrole cofactor F430: comparison of the forms bound to methyl coenzyme M reductase and protein free in cells of Methanobacterium thermoautotrophicum delta H. Biochemistry 23:801–804
Hausinger RP, Desguin B, Fellner M, Rankin JA, Hu J (2018) Nickel pincer nucleotide cofactor. Curr Opin Chem Biol 47:18–23
He MM, Clugston SL, Honek JF, Matthews BW (2000) Determination of the structure of Escherichia coli glyoxylase I suggests a structural basis for differential metal activation. Biochemistry 39:8719–8727
Heddle J, Scott DJ, Unzai S, Park S-Y, Tame JRH (2003) Crystal structures of the liganded and unliganded nickel-binding protein NikA from Escherichia coli. J Biol Chem 278:50322–50329
Herr CQ, Hausinger RP (2018) Amazing diversity in biochemical roles of Fe(II)/2-oxoglutarate oxygenases. Trends Biochem Sci 43:517–532
Higgins K (2019) Nickel metalloregulators and chaperones. Inorganics 7:104
Higgins KA, Carr CE, Maroney MJ (2012a) Specific metal recognition in nickel trafficking. Biochemistry 51:7816–7832
Higgins KA, Chivers PT, Maroney MJ (2012b) Role of the N-terminus in determining metal-specific responses in the E. coli Ni- and Co-responsive metalloregulator, RcnR. J Am Chem Soc 134:7081–7093
Higuchi Y, Yagi T, Yasuoka N (1997) Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis. Structure 5:1671–1680
Honek JF (2015) Glyoxalase biochemistry. Biomol Concepts 6:401–414
Honek JF (2017) Nickel glyoxalase I. In: Zamble D, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. The Royal Society of Chemistry, Cambridge
Howlett RM, Hughes BM, Hitchcock A, Kelly DJ (2012) Hydrogenase activity in the foodborne pathogen Campylobacter jejuni depends upon a novel ABC-type nickel transporter (NikZYXWV) and is SlyD-independent. Microbiology 158:1645–1655
Hu HQ, Huang H-T, Maroney MJ (2018) The Helicobacter pylori HypA·UreE2 complex contains a novel high-affinity Ni(II)-binding site. Biochemistry 57:2932–2942
Hurwitz J, Gold M, Anders M (1964) The enzymatic methylation of ribonucleic acid and deoxyribonucleic acid. IV. The properties of the soluble ribonucleic acid-methylating enzymes. J Biol Chem 239:3474–3482
Inoue M, Nakamoto I, Omae K, Oguro T, Ogata H, Yoshida T, Sako Y (2019) Structural and phylogenetic diversity of anaerobic carbon-monoxide dehydrogenases. Front Microbiol 9:3353
Iwig JS, Chivers PT (2009) DNA recognition and wrapping by Escherichia coli RcnR. J Mol Biol 393:514–526
Iwig JS, Chivers PT (2010) Coordinating intracellular nickel--metal-site structure-function relationships and the NikR and RcnR repressors. Nat Prod Rep 27:658–667
Iwig JS, Rowe JL, Chivers PT (2006) Nickel homeostasis in Escherichia coli - the rcnR-rcnA efflux pathway and its linkage to NikR function. Mol Microbiol 62:252–262
Iwig JS, Leitch S, Herbst RW, Maroney MJ, Chivers PT (2008) Ni(II) and Co(II) sensing by Escherichia coli RcnR. J Am Chem Soc 130:7592–7606
Iyaka YA (2011) Nickel in soils: a review of its distribution and impacts. Sci Res Essays 6:6774–6777
Jabri E, Karplus PA (1996) Structures of the Klebsiella aerogenes urease apoprotein and two active-site mutants. Biochemistry 35:10616–10626
Jabri E, Carr MB, Hausinger RP, Karplus PA (1995) The crystal structure of urease from Klebsiella aerogenes. Science 268:998–1004
Jacobi A, Rossman R, Böck A (1992) The hyp operon gene products are required for maturation of catalytically active hydrogenase isoenzymes in Escherichia coli. Arch Microbiol 158:444–451
Jeon WB, Cheng J, Ludden PW (2001) Purification and characterization of membrane-associated CooC protein and its functional role in the insertion of nickel into carbon monoxide dehydrogenase from Rhodospirillum rubrum. J Biol Chem 276:38602–38609
Jeoung J-H, Giese T, Grünwald M, Dobbek H (2009) CooC1 from Carboxydothermus hydrogenoformans is a nickel-binding ATPase. Biochemistry 48:11505–11513
Jeoung J-H, Giese T, Grünwald M, Dobbek H (2010) Crystal structure of the ATP-dependent maturation factor of Ni,Fe-containing carbon monoxide dehydrogenase. J Mol Biol 396:1165–1179
Jeoung J-H, Nianios D, Fetzner S, Dobbek H (2017) Quercetin 2,4-dioxygenase activates dioxygen in a side-on O2-Ni complex. Angew Chem Int Ed 55:3281–3284
Jia B, Jia X, Kim KH, Jeon CO (2017) Integrative view of 2-oxoglutarate/Fe(II)-dependent oxygenase diversity and functions in bacteria. Biochim Biophys Acta 1861:323–334
Jiang D, Zhao Y, Wang X, Fan J, Heng J, Liu X, Feng W, Kang X, Huang B, Liu J, Zhang XC (2013) Structure of the YajR transporter suggests a transport mechanism based on the conserved motif A. Proc Natl Acad Sci U S A 110:14664–14669
Johnson OE, Ryan KC, Maroney MJ, Brunold TC (2010) Spectroscopic and computational investigation of three Cys-to-Ser mutants of nickel superoxide dismutase: insight into the roles played by the Cys2 and Cys6 active-site residues. J Biol Inorg Chem 15:777–793
Joho M, Inouhe M, Tohoyama H, Murayama T (1990) A possible role of histidine in a nickel resistant mechanism of Saccharomyces cerevisiae. FEMS Microbiol Lett 66:333–338
Joho M, Ishikawa Y, Kunikane M, Inouhe M, Tohoyama H, Murayama T (1992) The subcellular distribution of nickel in Ni-sensitive and Ni-resistant strains of Saccharomyces cerevisiae. Microbios 71:149–159
Jones MD, Zamble DB (2018) Acid-responsive activity of the Helicobacter pylori metalloregulator NikR. Proc Natl Acad Sci U S A 115:8966–8971
Jones MD, Ademi I, Yin X, Gong Y, Zamble DB (2015) Nickel-responsive regulation of two novel Helicobacter pylori NikR-targeted genes. Metallomics 7:662–673
Ju T, Goldsmith RB, Chai SC, Maroney MJ, Pochapsky SS, Pochapsky TC (2006) One protein, two enzymes revisited: a structural entropy switch interconverts the two isoforms of acireductone dioxygenase. J Mol Biol 393:823–834
Jubier-Maurin V, Rodrigue A, Ouahrani-Bettache S, Layssac M, Mandrand-Bethelot M-A, Köhler S, Liautard J-P (2001) Identification of the nik gene cluster of Brucella suis: regulation and contribution to urease activity. J Bacteriol 183:426–434
Kalliri E, Grzyska PK, Hausinger RP (2005) Kinetic and spectroscopic investigation of CoII, NiII, and N-oxalylglycine inhibition of the FeII/a-ketoglutarate dioxygenase, TauD. Biochem Biophys Res Commun 338:191–197
Kaluarachchi H, Chan Chung KC, Zamble DB (2010) Microbial nickel proteins. Nat Prod Rep 27:681–694
Kaluarachchi H, Zhang JW, Zamble DB (2011) Escherichia coli SlyD, more than a Ni(II) reservoir. Biochemistry 50:10761–10763
Kasprzak KS, Salnikow K (2007) Nickel toxicity and carcinogenesis. In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in life sciences. Wiley, New York
Kerby RL, Ludden PW, Roberts GP (1997) In vivo nickel insertion into carbon monoxide dehydrogenase of Rhodosprillum rubrum: molecular and physiological characterization of cooCTJ. J Bacteriol 179:2259–2266
Kidd SP, Djoko KY, Ng J, Argente MP, Jennings MP, McEwan AG (2011) A novel nickel responsive MerR-like regulator, NimR, from Haemophilus influenzae. Metallomics 3:1009–1018
Kim E-J, Kim H-P, Hah YC, Roe J-H (1996) Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor. Eur J Biochem 214:178–185
Kim E-J, Chung H-J, Suh B, Hah YC, Roe J-H (1998a) Expression and regulation of the sodF gene encoding iron- and zinc-containing superoxide dismutase in Streptomyces coelicolor Müller. J Bacteriol 180:2014–2020
Kim E-J, Chung H-J, Suh B, Hah YC, Roe J-H (1998b) Transcriptional and post-transcriptional regulation by nickel of sodN gene encoding nickel-containing superoxide dismutase from Streptomyces coelicolor Müller. Mol Microbiol 27:187–195
Kim I-K, Yim Y-I, Kim Y-M, Lee J-W, Yim H-S, Kang S-O (2003a) CbiX-homologous protein (CbiXhp), a metal-binding protein, from Streptomyces seoulensis is involved in expression of nickel-containing superoxide dismutase. FEMS Microbiol Lett 228:21–26
Kim J-S, Kang S-O, Lee J-K (2003b) The protein complex composed of nickel-binding SrnQ and DNA binding motif-bearing SrnR of Streptomyces griseus represses sodF transcription in the presence of nickel ions. J Biol Chem 278:18455–18463
Kim JK, Mulrooney SB, Hausinger RP (2005) Biosynthesis of active Bacillus subtilis urease in the absence of known urease accessory proteins. J Bacteriol 187:7150–7154
Kim HM, Ahn B-E, Lee J-H, Roe J-H (2015) Regulation of a nickel-cobalt efflux system and nickel homeostasis in a soil actinobacterium Streptomyces coelicolor. Metallomics 7:702–709
King GM, Weber CF (2007) Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 5:107–118
Koch D, Nies DH, Grass G (2007) The RcnRA (YohLM) system of Escherichia coli: a connection between nickel, cobalt, and iron homeostasis. Biometals 20:759–771
Krüger M, Meyerdierks A, Glöckner FO, Amann R, Widdel F, Kube M, Reinhardt R, Kahnt J, Böcher R, Thauer RK, Shima S (2003) A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426:878–881
Kulathila R, Kulathila R, Indic M, van den Berg B (2011) Crystal structure of Escherichia coli CusC, the outer membrane component of a heavy metal efflux pump. PLoS One 6:e15610
Kumar V, Mishra RK, Kaur G, Dutta D (2017) Cobalt and nickel impair DNA metabolism by the oxidative stress independent pathway. Metallomics 9:1596–1609
Kung Y, Drennan CL (2017) One-carbon chemistry of nickel-containing carbon monoxide dehydrogenase and acetyl-CoA synthase. In: Zamble D, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. Royal Society of Chemistry, Cambridge
Kurzer F, Sanderson PM (1956) Urea in the history of organic chemistry. J Chem Ed 33:452–459
Kusters JG, Van Vliet AHM, Kuipers EJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19:449–490
Kwon S, Nishitani Y, Watanabe S, Hirao Y, Imanaka T, Kanai T, Atomi H, Miki K (2016) Crystal structure of a [NiFe] hydrogenase maturation protease HybD from Thermococcus kodakarensis KOD1. Proteins 84:1321–1327
Kwon S, Watanabe S, Nishitani Y, Kawashima T, Kanai T, Atomi H, Miki K (2018) Crystal structures of a [NiFe] hydrogenase large subunit HyhL in an immature state in complex with a Ni chaperone HypA. Proc Natl Acad Sci U S A 115:7045–7050
Labigne A, Cussac V, Courcoux P (1991) Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity. J Bacteriol 173:1920–1931
Lacasse MJ, Zamble DB (2016) [NiFe]-hydrogenase maturation. Biochemistry 55:1689–1701
Lam R, Romanov V, Johns K, Battaile K, Wu-Brown J, Guthrie JL, Hausinger RP, Pai E, Chirgadze NY (2010) Crystal structure of a truncated urease accessory protein UreF from Helicobacter pylori. Proteins 78:2839–2848
Laso-Pérez R, Wegener G, Knittel K, Widdel F, Harding KJ, Krukenberg V, Meier DV, Richter M, Tegetmeyer HE, Riedel D, Richnow H-H, Adrian L, Reemtsma T, Lechtenfeld OJ, Musat F (2016) Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature 539:396–401
Laso-Pérez R, Hahn C, van Vliet DM, Tegetmeyer HE, Schubotz F, Smit NT, Pape T, Sahling H, Bohrmann G, Boetius A, Knittel K, Wegener G (2019) Anaerobic degradation of non-methane alkanes by “Candidatus Methanoliparia” in hydrocarbon seeps of the gulf of Mexico. mBio 10:e01814–e01819
Leach MR, Zamble DB (2007) Metallocenter assembly of the hydrogenase enzymes. Curr Opin Chem Biol 11:159–165
Leach MR, Zhang JW, Zamble DB (2007) The role of complex formation between the Escherichia coli hydrogenase factors HypB and SlyD. J Biol Chem 282:16177–16186
Lebrette H, Iannello M, Fontecilla-Camps JC, Cavazza C (2013) The binding mode of Ni-(L-His)2 in NikA revealed by X-ray crystallography. J Inorg Biochem 121:16–18
Lebrette H, Brochier-Armanet C, Zambelli B, de Reuse H, Borezée-Durant E, Ciurli S, Cavazza C (2014) Promiscuous nickel import in human pathogens: structure, thermodynamics, and evolution of extracytoplasmic nickel-binding proteins. Structure 22:1421–1432
Lebrette H, Borezee-Durant E, Martin L, Richaud P, Boeri Erba E, Cavazza C (2015) Novel insights into nickel import in Staphylococcus aureus: the positive role of free histidine and structural characterization of a new thiazolidine-type nickel chelator. Metallomics 7:613–621
Leclere V, Boiron P, Blondeau R (1999) Diversity of superoxide-dismutases among clinical and soil isolates of Streptomyces species. Curr Microbiol 39:365–368
Lee MH, Mulrooney SB, Renner MJ, Markowicz Y, Hausinger RP (1992) Klebsiella aerogenes urease gene cluster: sequence of ureD and demonstration that four accessory genes (ureD, ureE, ureF, and ureG) are involved in nickel metallocenter biosynthesis. J Bacteriol 174:4324–4330
Lee MH, Pankratz HS, Wang S, Scott RA, Finnegan MG, Johnson MK, Ippolito JA, Christianson DW, Hausinger RP (1993) Purification and characterization of Klebsiella aerogenes UreE protein: a nickel-binding protein that functions in urease metallocenter assembly. Protein Sci 2:1042–1052
Lee CW, Chakravorty DK, Chang F-MJ, Reyes-Caballero H, Ye Y, Merz KM Jr, Giedroc DP (2012) Solution structure of Mycobacterium tuberculosis NmtR in the apo state: insights into Ni(II)-mediated allostery. Biochemistry 51:2619–2629
Lemaire ON, Wagner T (2020) Gas channel rerouting in a primordial enzyme: structure insights of the carbon-monoxide dehydrogenase/acetyl-CoA synthase complex from the acetogen Clostridium autoethanogenum. Biochim Biophys Acta 1862:148330
Lenz O, Friedrich B (1998) A novel multicomponent regulatory system mediates H2 sensing in Alcaligenes eutrophus. Proc Natl Acad Sci U S A 95:12474–12479
Li Y, Zamble DB (2009) Nickel homeostasis and nickel regulation: an overview. Chem Rev 109:4617–4643
Li C, Vavra JW, Carr CE, Huang H-T, Maroney MJ, Wilmot CM (2020) Complexation of the nickel and cobalt transcriptional regulator RcnR with DNA. Acta Crystallogr F76:25–30
Liesegang H, Lemke K, Siddiqui RA, Schlegel HG (1993) Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34. J Bacteriol 175:767–778
Loke H-K, Lindahl PA (2003) Identification and preliminary characterization of AcsF, a putative Ni-insertase used in the biosynthesis of acetyl-CoA synthase from Clostridium thermoaceticum. J Inorg Biochem 93:33–40
Loke H-K, Bennett GN, Lindahl PA (2000) Active acetyl-CoA synthase from Clostridium thermoaceticum obtained by cloning and heterologous expression of acsAB in Escherichia coli. Proc Natl Acad Sci U S A 97:12530–12535
Long F, Su C-C, Zimmermann MT, Boyken SE, Rajashankar KR, Jernigan RL, Yu EW (2010) Crystal structures of the CusA efflux pump suggest methionine-mediated metal transport. Nature 467:484–488
Lopez-Maury L, Garcia-Dominguez M, Florencio FJ, Reyes JC (2002) A two-component signal transduction system involved in nickel sensing in the cyanobacterium Synechocystis sp. PCC 6803. Mol Microbiol 43:247–256
Louwrier A, Knowles CJ (1996) The purification and characterization of a novel D(−)-specific carbamoylase enzyme from Agrobacterium sp. Enzym Microb Technol 19:562–571
Lu M, Chai J, Fu D (2009) Structural basis for autoregulation of the zinc transporter YiiP. Nat Struct Mol Biol 16:1063–1068
Lu M, Jiang Y-L, Wang S, Jin H, Zhang R-G, Virolle M-J, Chen Y, Zhou C-Z (2014) Streptomyces coelicolor SCO4226 is a nickel binding protein. PLoS One 9:e109660
Lubitz W, Ogata H, Rüdiger O, Reijerse E (2014) Hydrogenases. Chem Rev 114:4081–4148
Lutz A, Jacobi A, Schlensog V, Böhm R, Sawers G, Böck A (1991) Molecular characterization of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes in Escherichia coli. Mol Microbiol 5:123–135
Lyu Z, Shao N, Chou C-W, Shi H, Patel R, Duin EC, Whitman WB (2020) Posttranslational modification of arginine in methyl coenzyme M reductase has a profound impact on both methanogenesis and growth of Methanococcus maripaludis. J Bacteriol 202:e00654–e00619
Macomber L, Hausinger RP (2011) Mechanisms of nickel toxicity in microorganisms. Metallomics 3:1153–1162
Macomber L, Elsey SP, Hausinger RP (2011) Fructose-1,6-bisphosphate aldolase (class II) is the primary site of nickel toxicity in Escherichia coli. Mol Microbiol 82:1291–1300
Maeda M, Hidaka M, Nakamura A, Masaki H, Uozumi T (1994) Cloning, sequencing, and expression of thermophilic Bacillus sp. strain TB-90 urease gene complex in Escherichia coli. J Bacteriol 176:432–442
Maillard AP, Girard E, Ziani W, Petit-Hartlein I, Kahn R, Covès J (2014) The crystal structure of the anti-s factor CnrY in complex with the s factor CnrH shows a new structural class of anti-s factors targeting extracytoplasmic function s factors. J Mol Biol 426:2313–2327
Maillard AP, Künnemann S, Grobe C, Volbeda A, Schleuder G, Petit-Hartlein I, De Rosny E, Nies D, Covès J (2015) Response of CnrX from Cupriavidus metallidurans CH34 to nickel binding. Metallomics 7:622–631
Manley OM, Myers PD, Toney DJ, Bolling KF, Rhodes LC, Gasparik JL, Grossoehme NE (2020) Evaluation of the regulatory model for Ni2+ sensing by Nur from Streptomyces coelicolor. J Inorg Biochem 203:110859
Maratea D, Young K, Young R (1985) Deletion and fusion analysis of the phage phi X174 lysis gene E. Gene 40:39–46
Marcus EA, Scott DR (2001) Cell lysis is responsible for the appearance of extracellular urease in Helicobacter pylori. Helicobacter 6:93–99
Maroney MJ, Ciurli S (2014) Nonredox nickel enzymes. Chem Rev 114:4206–4228
Marques MC, Coelho R, De Lacey AI, Pereira IA, Matias PM (2010) The three-dimensional structure of [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough: a hydrogenase without a bridging ligand in the active site in its oxidized, “as isolated” state. J Mol Biol 396:893–907
Marrero J, Auling G, Coto O, Nies DH (2007) High-level resistance to cobalt and nickel but probably no transenvelope efflux: metal resistance in the Cuban Serratia marcescens strain C-1. Microb Ecol 53:123–133
Martin-Diaconescu V, Joseph C, Boer JL, Mulrooney SB, Hausinger RP, Maroney MJ (2017) Non-thiolate ligation of nickel by nucleotide-free UreG of Klebsiella aerogenes. J Biol Inorg Chem 22:497–503
Masetti M, Bertazzo M, Recanatini M, Ciurli S, Musiani F (2021) Probing the transport of Ni (II) ions through the internal tunnels of the Helicobacter pylori UreDFG multimeric protein complex. J Inorg Biochem 223:111554. https://doi.org/10.1016/j.jinorgbio.2021.111554
Matias PM, Soares CM, Saraiva LM, Coelho R, Morais J, Le Gall J, Carrondo MA (2001) [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structures determination and refinement at 1.8 Å and modeling studies of its interaction with the tetrahaem cytochrome c3. J Biol Inorg Chem 6:63–81
Maynard EL, Lindahl PA (1999) Evidence of a molecular tunnel connecting the active sites for CO2 reduction and acetyl-CoA synthesis in acetyl-CoA synthase from Clostridium thermoaceticum. J Am Chem Soc 121:9221–9222
Mayr S, Latkoczy C, Krüger M, Günther D, Shima S, Thauer RK, Widdel F, Jaun B (2008) Structure of an F430 variant from archaea associated with anaerobic oxidation of methane. J Am Chem Soc 130:10758–10767
Mazzei L, Muslani F, Ciurli S (2020) The structure-based reaction mechanism of urease, a nickel dependent enzyme: tale of a long debate. J Biol Inorg Chem 25:829–845
Mazzei L, Musiani F, Żerko S, Koźminski W, Cianci M, Beniamino Y, Ciurli S, Zambelli B (2021) Structure, dynamics, and function of SrnR, a transcription factor for nickel-dependent gene expression. Metallomics 13(12):mfab069. https://doi.org/10.1093/mtomcs/mfab069
McLean RJC, Nickel JC, Cheng K-J, Costerton JW (1988) The ecology and pathogenicity of urease-producing bacteria in the urinary tract. Crit Rev Microbiol 16:37–79
McLean RJC, Beauchemin D, Clapham L, Beveridge TJ (1990) Metal-binding characteristics of the gamma-glutamyl capsular polymer of Bacillus licheniformis ATCC 9945. Appl Environ Microbiol 56:3671–3677
McMillan DJ, Mau M, Walker MJ (1998) Characterization of the urease gene cluster in Bordetella bronchiseptica. Gene 208:243–251
Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, van Gijsegem F (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334
Merloni A, Dobrovolska O, Zambelli B, Agostini F, Bazzani M, Musiani F, Ciurli S (2014) Molecular landscape of the interaction between the urease accessory proteins UreE and UreG. Biochim Biophys Acta 1844:1662–1674
Merrouch M, Benvenuti M, Lorenzi M, Léger C, Fourmond V, Dementin S (2018) Maturation of the [Ni-4Fe-4S] active site of carbon monoxide dehydrogenases. J Biol Inorg Chem 23:613–620
Meuer J, Bartoschek S, Koch J, Kunkel A, Hedderich R (1999) Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri. Eur J Biochem 265:325–335
Miki K, Atomi H, Watanabe B (2020) Structural insight into [NiFe] hydrogenase maturation by transient complexes between Hyp proteins. Acc Chem Res 53:875–886
Miquel P (1890) C R Acad Sci 111:397
Miraula M, Ciurli S, Zambelli B (2015) Intrinsic disorder and metal binding in UreG proteins from Archae hyperthermophiles: GTPase enzymes involved in the activation of Ni(II) dependent urease. J Biol Inorg Chem 20:739–755
Mobley HLT, Hausinger RP (1989) Microbial ureases: significance, regulation, and molecular characterization. Microbiol Rev 53:85–108
Mobley HLT, Garner RM, Bauerfeind P (1995a) Helicobacter pylori nickel-transport gene nixA: synthesis of catalytically active urease in Escherichia coli independent of growth conditions. Mol Microbiol 16:97–109
Mobley HLT, Island MD, Hausinger RP (1995b) Molecular biology of microbial ureases. Microbiol Rev 59:451–480
Moncrief MBC, Hausinger RP (1996) Purification and activation properties of UreD-UreF-urease apoprotein complexes. J Bacteriol 178:5417–5421
Moncrief MBC, Hausinger RP (1997) Characterization of UreG, identification of a UreD-UreF-UreG complex, and evidence suggesting that a nucleotide-binding site in UreG is required for in vivo metallocenter assembly of Klebsiella aerogenes urease. J Bacteriol 179:4081–4086
Moore SJ, Sowa ST, Schuchardt C, Deery E, Lawrence AD, Ramos JV, Billig S, Birkemeyer C, Chivers PT, Howard MJ, Rigby SE, Layer G, Warren MJ (2017) Elucidation of the biosynthesis of the methane catalyst coenzyme F430. Nature 543:78–82
Muller C, Bahlawane C, Aubert S, Delay CM, Schauer K, Michaud-Soret I, De Reuse H (2011) Hierarchical regulation of the NikR-mediated nickel response in Helicobacter pylori. Nucleic Acids Res 39:7564–7575
Mulrooney SB, Hausinger RP (1990) Sequence of the Klebsiella aerogenes urease genes and evidence for accessory proteins facilitating nickel incorporation. J Bacteriol 172:5837–5843
Mulrooney SB, Ward SK, Hausinger RP (2005) Purification and properties of the Klebsiella aerogenes UreE metal-binding domain, a functional metallochaperone of urease. J Bacteriol 187:3581–3585
Munkelt D, Grass G, Nies DH (2004) The chromosomally encoded cation diffusion facilitator proteins DmeF and FieF from Wautersia metallidurans CH34 are transporters of broad metal specificity. J Bacteriol 186:8036–8043
Muraki N, Ishii K, Uchiyama S, Itoh SG, Okumura H, Aono S (2019) Structural characterization of HypX responsible for CO biosynthesis in the maturation of NiFe-hydrogenase. Commun Biol 2:385
Musiani F, Zambelli B, Stola M, Ciurli S (2004) Nickel trafficking: insights into the fold and function of UreE, a urease metallochaperone. J Inorg Biochem 98:803–813
Musiani F, Zambelli B, Bazzani M, Mazzei L, Ciurli S (2015) Nickel-responsive transcriptional regulators. Metallomics 7:1305–1318
Navarro C, Wu L-F, Mandrand-Berthelot M-A (1993) The nik operon of Escherichia coli encodes a periplasmic binding-protein-dependent transport system for nickel. Mol Microbiol 9:1181–1191
Nayak DD, Mahanta N, Mitchell DA, Metcalf WW (2017) Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic archaea. elife 6:e29218
Nayak DD, Liu A, Agrawal N, Rodriquez-Carerro R, Dong S-H, Mitchell DA, Nair SK, Metcalf WW (2020) Functional interactions between posttranslationally modified amino acids of methyl-coenzyme M reductase in Methanosarcina acetivorans. PLoS Biol 18:e3000507
Nevarez JL, Turmo A, Hu J, Hausinger RP (2020) Biochemical pincer complexes. ChemCatChem 12:4242–4254
Nianios D, Thierbach S, Steimer L, Lulchev P, Klostermeier D, Fetzner S (2015) Nickel quercetinase, a “promiscuous” metalloenzyme: metal incorporation and metal ligand substitution studies. BMC Biochem 16:10
Nielubowicz GR, Mobley HLT (2010) Host-pathogen interactions in the urinary tract interaction. Nat Rev Urol 7:430–441
Nies DH, Covès J, Sawers RG (2017) Cross-talk between nickel and other metals in microbial systems. In: Zamble DB, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. Royal Society of Chemistry, Cambridge
Niki E, Yoshida Y, Saito Y, Noguchi N (2005) Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem Biophys Res Commun 338:668–676
Nim YS, Wong K-B (2019) The maturation pathway of nickel urease. Inorganics 7:85
Nishimura K, Igarashi K, Kakinuma Y (1998) Proton gradient-driven nickel uptake by vacuolar membrane vesicles of Saccharomyces cerevisiae. J Bacteriol 180:1962–1964
Noll KN, Rinehart KL Jr, Tanner RS, Wolfe RS (1986) Structure of component B (7-mercaptoheptanoylthreonine phosphate) of the methylcoenzyme M methylreductase system of Methanobacterium thermoautotrophicum. Proc Natl Acad Sci U S A 83:4238–4242
Norsworthy AN, Pearson MM (2017) From catheter to kidney stone: the uropathogenic lifestyle of Proteus mirabilis. Trends Microbiol 25:304–315
Nriagu JO (1980) Nickel in the environment. Wiley, New York
Ogata H, Kellers P, Lubitz W (2010) The crystal structure of the [NiFe] hydrogenase from the photosynthetic bacterium Allochromatium vinosum: characterization of the oxidized enzyme (Ni-A state). J Mol Biol 402:428–444
Ogata H, Nishikawa K, Lubitz W (2015) Hydrogens detected by subatomic resolution protein crystallography in a [NiFe] hydrogenase. Nature 520:571–574
Ogata H, Lubitz W, Higuchi Y (2016) Structure and function of [NiFe] hydrogenases. J Biochem 160:251–258
Olson JW, Maier RJ (2000) Dual roles of Bradyrhizobium japonicum nickelin protein in nickel storage and GTP-dependent Ni mobilization. J Bacteriol 182:1702–1705
Olson JW, Mehta NS, Maier RJ (2001) Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori. Mol Microbiol 39:176–182
Outten CE, O’Halloran TV (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492
Padmanabhan PK, Mukherjee A, Singh S, Chattopadhyaya S, Gowri VS, Myler PJ, Srinivasan N, Mahubala R (2005) Glyoxylase I from Leishmania donovani: a potential target for anti-parasite drug. Biochem Biophys Res Commun 337:1237–1248
Pal A, Paul AK (2010) Nickel uptake and intracellular localization in Cupriavidus pauculus KPS 201, native to ultramafic ecosystem. Adv Biosci Biotechnol 1:276–280
Palmgren MG, Nissen P (2011) P-type ATPases. Annu Rev Biophys 40:243–266
Palombo M, Bonucci A, Etienne E, Ciurli S, Uversky VN, Guigliarelli B, Belle V, Mileo E, Zambelli B (2017) The relationship between folding and activity in UreG, an intrinsically disordered enzyme. Sci Rep 7:5977
Paraszkiewicz K, Bernat P, Naliwajski M, Dlugonski J (2010) Lipid peroxidation in the fungus Curvularia lunata exposed to nickel. Arch Microbiol 192:135–141
Park I-S, Carr MB, Hausinger RP (1994) In vitro activation of urease apoprotein and role of UreD as a chaperone required for nickel metallocenter assembly. Proc Natl Acad Sci U S A 91:3233–3237
Park JE, Schlegel H-G, Rhie HG, Lee HS (2004) Nucleotide sequence and expression of the ncr nickel and cobalt resistance in hafnia alvei 5-5. Int Microbiol 7:27–34
Park J-S, Lee S-J, Rhie H-G, Lee H-S (2008) Characterization of a chromosomal nickel resistance determinant from Klebsiella oxytoca CCUG 15788. J Microbiol Biotechnol 18:1040–1043
Pasteur L (1860) De l’origine des ferments, etc. C R Acad Sci 50:849
Pearce DA, Sherman F (1999) Toxicity of copper, cobalt, and nickel salts is dependent on histidine metabolism in the yeast Saccharomyces cerevisiae. J Bacteriol 181:4774–4779
Pearson MA, Michel LO, Hausinger RP, Karplus PA (1997) Structure of Cys319 variants and acetohydroxamate-inhibited Klebsiella aerogenes urease. Biochemistry 36:8164–8172
Pennella MA, Shokes JE, Cosper NJ, Scott RA, Giedroc DP (2003) Structural elements of metal selectivity in metal sensor proteins. Proc Natl Acad Sci U S A 100:3713–3718
Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM, Broderick JB, King PW, Adams MWW (2015) [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. Biochim Biophys Acta 1853:1350–1369
Petkun S, Shi R, Li Y, Asinas A, Munger C, Zhang L, Waclawek M, Soboh B, Sawers RG, Cygler M (2011) Structure of hydrogenase maturation protein HypB with reaction intermediates shows two active sites. Structure 19:1773–1783
Pfaltz A, Livingston DA, Jaun B, Diekert G, Thauer RK, Eschenmoser A (1985) Factor F430 from methanogenic bacteria: on the nature of the isolation artifacts of F430, a contribution to the chemistry of F430 and the conformational stereochemistry of the ligand periphery of hydroporphinoid nickel(II) complexes. Helv Chim Acta 68:1338–1358
Pfaltz A, Kobelt A, Hüster R, Thauer RK (1987) Biosynthesis of coenzyme F430 in methanogenic bacteria. Identification of 15,173-seco-F430-173-acid as an intermediate. Eur J Biochem 170:459–467
Phillips CM, Schreiter ER, Guo Y, Wang SC, Zamble DB, Drennan CL (2008) Structural basis of the metal specificity for nickel regulatory protein NikR. Biochemistry 47:1938–1946
Phillips CM, Schreiter ER, Stultz CM, Drennan CL (2010) Structural basis of low-affinity nickel binding to the nickel-responsive transcription factor NikR from Escherichia coli. Biochemistry 49:7830–7838
Pierik AJ, Roseboom W, Happe RP, Bagley KA, Albracht SPJ (1999) Carbon monoxide and cyanide as intrinsic ligands to iron in the active site of [NiFe]-hydrogenases -- NiFe(CN)2CO, biology’s way to activate H2. J Biol Chem 274:3331–3337
Pinkett HW, Lee AT, Lum P, Locher KP, Rees DC (2007) An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science 315:373–377
Pinske C, Sargent F, Sawers RG (2015) SlyD-dependent nickel delivery limits maturation of [NiFe]-hydrogenases in late-stationary phase Escherichia coli cells. Metallomics 7:683–690
Pochapsky TC, Pochapsky SS, Ju T, Mo H, Al-Mjeni F, Maroney MJ (2002) Modeling and experiment yields the structure of acireductone dioxygenase from Klebsiella pneumoniae. Nat Struct Biol 9:966–972
Pochapsky SS, Sunshine JC, Pochapsky TC (2008) Completing the circuit: direct-observe 13C, 15N double-quantum spectroscopy permits sequential resonance assignments near a paramagnetic center in acireductone dioxygenase. J Am Chem Soc 130:2156–2157
Pompidor G, Maillard AP, Girard E, Gambarelli S, Kahn R, Covès J (2008) X-ray structure of the metal-sensor CnrX in both the apo- and copper-bound forms. FEBS Lett 582:3954–3958
Quiroz-Valenzuela S, Sukuru SCK, Hausinger RP, Kuhn LA, Heller WT (2008) The structure of urease activation complexes examined by flexibility analysis, mutagenesis, and small-angle X-ray scattering. Arch Biochem Biophys 480:51–57
Ragsdale SW, Raugei S, Ginovska B, Wongnate T (2017) Biochemistry of methyl-coenzyme M reductase. In: Zamble D, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. Royal Society of Chemistry, Cambridge
Ragusa S, Blanquet S, Meinnel T (1998) Control of peptide deformylase activity by metal cations. J Mol Biol 280:515–523
Rai R, Saraswat VA, Dhiman RK (2015) Gut microbiota: its role in hepatic encephalopathy. J Clin Exp Hepatol 5:S29–S36
Raimunda D, Long JE, Sassetti CM, Argüello JM (2012) Role in metal homeostasis of CtpD, a Co2+ transporting P1B4-ATPase of Mycobacterium smegmatis. Mol Microbiol 84:1139–1149
Rajagopalan PT, Pei D (1998) Oxygen-mediated inactivation of peptide deformylase. J Biol Chem 273:22305–22310
Randhawa VK, Zhou F, Jin X, Nalewajko C, Kushner DJ (2001) Role of oxidative stress and thiol antioxidant enzymes in nickel toxicity and resistance in strains of the green alga Scenedesmus acutus f. alternans. Can J Microbiol 47:987–993
Rankin JA, Mauban RC, Fellner M, Desguin B, McCracken J, Hu J, Varganov SA, Hausinger RP (2018) Lactate racemase nickel-pincer cofactor operates by a proton-coupled hydride transfer mechanism. Biochemistry 57:3244–3251
Rankin JA, Chatterjee S, Tariq Z, Lagishetty S, Desguin B, Hu J, Hausinger RP (2021) The LarB carboxylase/hydrolase forms a transient cysteinyl-pyridine intermediate during nickel-pincer nucleotide cofactor biosynthesis. Proc Natl Acad Sci 118(39):e2106202118. https://doi.org/10.1073/pnas.2106202118
Ravichandran R, Hemaasri S, Cameotra SS, Jayaprakash NS (2015) Purification and characterization of an extracellular uricase from a new isolate of Sphingobacterium thalpophilum (VITPCB5). Protein Expr Purif 114:136–142
Reissmann S, Hochleitner E, Wang H, Paschos A, Lottspeich F, Glass RS, Böck A (2003) Taming of a poison: biosynthesis of the NiFe-hydrogenase cyanide ligands. Science 299:1067–1070
Remaut H, Safarof N, Ciurli S, Van Beeumen J (2001) Structural basis for Ni2+ transport and assembly of the urease active site by the metallo-chaperone UreE from Bacillus pasteurii. J Biol Chem 276:49365–49370
Remy L, Carriére M, Derré-Bobillot A, Martini C, Sanguinetti M, Borezée-Durant E (2013) The Staphylococcus aureus Opp1 ABC transporter imports nickel and cobalt in zinc-depleted conditions and contributes to virulence. Mol Microbiol 87:730–743
Reyes-Caballero H, Lee CW, Giedroc DP (2011) Mycobacterium tuberculosis NmtR harbors a nickel sensing site with parallels to Escherichia coli RcnR. Biochemistry 50:7941–7952
Righetto RD, Anton L, Adaixo R, Jakob RP, Zivanov J, Mahi M-A, Ringler P, Schwede T, Maier T, Stahlberg H (2020) High-resolution cryo-EM structure of urease from the pathogen Yersinia enterocolitica. Nat Commun 11:5101
Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T (2006) Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J Bacteriol 188:317–327
Rodionova IA, Scott DA, Grishin NV, Osterman AL, Rodionov DA (2012) Tagaturonate-fructuronate epimerase UxaE, a novel enzyme in the hexuronate catabolic network in Thermotoga maritima. Environ Microbiol 14:2920–2934
Rodrigue A, Effantin G, Mandrand-Bethelot M-A (2005) Identification of rcnA (yohM), a nickel and cobalt resistance gene in Escherichia coli. J Bacteriol 187:2912–2916
Rodrigue A, Albareda M, Mandrand-Berthelot M-A, Palacios J (2017) Nickel in microbial physiology--from single proteins to complex trafficking systems: nickel import/export. In: Zamble DB, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. Royal Society of Chemistry, Cambridge
Rospert S, Linder D, Ellermann J, Thauer RK (1990) Two genetically distinct methyl-coenzyme M reductases in Methanobacterium thermoautotrophicum strain Marburg and DH. Eur J Biochem 194:871–877
Rubio-Sanz L, Prieto RI, Imperial J, Palacios JM, Brito B (2013) Functional and expression analysis of the metal inducible dmeRF system from Rhizobium leguminosarum bv. viciae. Appl Environ Microbiol 79:6414–6422
Ryan KC, Johnson OE, Cabelli DE, Brunold TC, Maroney MJ (2010) Nickel superoxide dismutase: structural and functional roles of Cys2 and Cys6. J Biol Inorg Chem 15:795–807
Sachs G, Scott D, Weeks D, Melchers K (2002) The compartment buffered by the urease of Helicobacter pylori: cytoplasm or periplasm? Trends Microbiol 10:217–219
Saier MH Jr, Beatty JT, Goffeau A, Harley KT, Heijne WH, Huang SC, Jack DL, Jahn PS, Lew K, Liu J, Pao SS, Paulsen IT, Tseng TT, Virk PS (1999) The major facilitator superfamily. J Mol Microbiol Biotechnol 1:257–279
San Martin-Uriz P, Mirete S, Alcolea PJ, Gomez MJ, Amils R, Gonzalez-Pastor JE (2014) Nickel-resistance determinants in Acidiphilum sp. PM identified by genome-wide functional screening. PLoS One 9:e95041
Sar P, Kazy SK, Singh SP (2001) Intracellular nickel accumulation by Pseudomonas aeruginosa and its chemical nature. Lett Appl Microbiol 32:257–261
Sargent F (2016) The model [NiFe]-hydrogenases of Escherichia coli. Adv Microb Physiol 68:433–507
Sasaki D, Watanabe B, Matsumi R, Shoji T, Yasukochi A, Tagashira K, Fukuda W, Kanai T, Atomi H, Imanaka T, Miki K (2013) Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturation. J Mol Biol 425:1627–1640
Sato K, Okuba A, Yamazaki S (1998) Characterization of a multi-copper enzyme, nitrous oxide reductase, from Rhodobacter sphaeroides f. sp. denitrificans. J Biochem 124:51–54
Sawers RG, Pinske C (2017) NiFe-hydrogenase assembly. In: Johnson MK, Scott RA (eds) Encyclopedia of inorganic and bioinorganic chemistry. Wiley
Saylor Z, Maier R (2018) Helicobacter pylori nickel storage proteins: recognition and modulation of diverse metabolic targets. Microbiology 164:1059–1068
Schaab MR, Barney BM, Francisco WA (2006) Kinetic and spectroscopic studies on the quercetin 2,3-dioxygenase from Bacillus subtilis. Biochemistry 45:1009–1016
Schäfer C, Bommer M, Hennig SE, Jeoung J-H, Dobbek H, Lenz O (2016) Structure of an actinobacterial-type [NiFe]-hydrogenase reveals insight into O2-tolerant H2 oxidation. Structure 24:285–292
Schauer K, Gouget B, Carrière M, Labigne A, de Reuse H (2007) Novel nickel transport mechanism across the bacterial outer membrane energized by the TonB/ExbB/ExbD machinery. Mol Microbiol 63:1054–1068
Scheller S, Goenrich M, Boecher R, Thauer RK, Jaun B (2010) The key nickel enzyme of methanogenesis catalyzes the anaerobic oxidation of methane. Nature 465:606–608
Schneider J, Kaltwasser H (1984) Urease from Arthrobacter oxydans, a nickel-containing enzyme. Arch Microbiol 139:355–360
Schreiter ER, Sintchak MD, Guo Y, Chivers PT, Sauer RT, Drennan CL (2003) Crystal structure of the nickel-responsive transcriptional factor NikR. Nat Struct Biol 10:794–799
Schreiter ER, Wang SC, Zamble DB, Drennan CL (2006) NikR-operator complex structure and the mechanism of repressor activation by metal ions. Proc Natl Acad Sci U S A 103:13676–13681
Schulz A-C, Frielingsdorf S, Pommerening P, Lauterbach L, Bistoni G, Neese F, Oestreich M, Lenz O (2020) Formyltetrahydrofolate decarbonylase synthesizes the active site CO ligand of O2-tolerant [NiFe] hydrogenase. J Am Chem Soc 142:1457–1464
Sebbane F, Mandrand-Bethelot M-A, Simonet M (2002) Genes encoding specific nickel transport systems flank the chromosomal urease locus of pathogenic Yersiniae. J Bacteriol 184:5706–5713
Seffernick JL, McTavish H, Osbourne JP, de Souza ML, Sadowsky MJ, Wackett LP (2002) Atrazine chlorohydrolase from pseudomonas sp. strain ADP is a metalloenzyme. Biochemistry 41:14430–14437
Selmer T, Kahn J, Goubeaud M, Shima S, Grabarse W, Ermler U, Thauer RK (2000) The biosynthesis of methylated amino acids in the active site region of methyl-coenzyme M reductase. J Biol Chem 275:3755–3760
Senger M, Stripp ST, Soboh B (2017) Proteolytic cleavage orchestrates cofactor insertion and protein assembly in [NiFe]-hydrogenase biosynthesis. J Biol Chem 292:11670–11681
Seravalli J, Ragsdale SW (2000) Channeling of carbon monoxide during anaerobic carbon dioxide fixation. Biochemistry 39:1274–1277
Seshadri S, Benoit SL, Maier RJ (2007) Roles of His-rich Hpn and Hpn-like proteins in Helicobacter pylori nickel physiology. J Bacteriol 189:4120–4126
Shafaat HS, Rüdiger O, Ogata H, Lubitz W (2013) [NiFe] hydrogenases: a common active site for hydrogen metabolism under diverse conditions. Biochim Biophys Acta 1827:986–1002
Shaik MM, Cendron L, Salamina M, Ruzzene M, Zanotti G (2014) Helicobacter pylori periplasmic receptor CeuE (HP1561) modulates its nickel affinity via organic metallophores. Mol Microbiol 91:724–735
Sheng Y, Abreu IA, Cabelli DE, Maroney MJ, Miller A-F, Teixeira M, Valentine JS (2014) Superoxide dismutases and superoxide reductases. Chem Rev 114:3854–3918
Shi R, Munger C, Asinas A, Benoit SL, Miller E, Matte A, Maier RJ, Cygler M (2010) Crystal structures of apo and metal-bound forms of the UreE protein from Helicobacter pylori: role of multiple metal binding sites. Biochemistry 49:7080–7088
Shima S, Thauer RK (2005) Methyl-coenzyme M reductase and anaerobic oxidation of methane in methanotrophic archaea. Curr Opin Microbiol 8:643–648
Shima S, Krueger M, Weingert T, Demmer U, Kahnt J, Thauer RK, Ermler U (2012) Structure of a methyl-coenzyme M reductase from Black Sea mats that oxidize methane anaerobically. Nature 481:98–101
Shomura Y, Higuchi Y (2012) Structural basis for the reaction mechanism of S-carbamoylation of HypE by HypF in the maturation of [NiFe]-hydrogenases. J Biol Chem 287:28409–28419
Shomura Y, Yoon K-S, Nishihara H, Higuchi Y (2011) Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase. Nature 479:253–256
Shomura Y, Taketa M, Nakashima H, Tai H, Nakagawa H, Ikeda H, Ishii M, Igarashi Y, Nishihara H, Yoon K-S, Ogo S, Hirota S, Higuchi Y (2017) Structural basis of the redox switches in the NAD+-reducing soluble [NiFe]-hydrogenase. Science 357:928–932
Siddiqui RA, Schlegel HG (1987) Plasmid pMOL28-mediated inducible nickel resistance in Alcaligenes eutrophus strain CH34. FEMS Microbiol Lett 43:9–13
Simitsopoulou M, Vafopoulou A, Choli-Papadopoulou T, Alichanidis E (1997) Purification and partial characterization of a tripeptidase from Pediococcus pentosaceus K9.2. Appl Environ Microbiol 63:4872–4876
Slotboom DJ (2014) Structural and mechanistic insights into prokaryotic energy-coupling factor transporters. Nat Rev Microbiol 12:79–87
Smith DH (1967) R factors mediate resistance to mercury, nickel and cobalt. Science 156:1114–1116
Snavely MD, Gravina SA, Cheung TT, Miller CG, Maguire ME (1991) Magnesium transport in Salmonella typhimurium. Regulation of mgtA and mgtB expression. J Biol Chem 266:824–829
Snow ET, Xu LS, Kinney PL (1993) Effects of nickel ions on polymerase activity and fidelity during DNA replication in vitro. Chem Biol Interact 88:155–173
Song HK, Mulrooney SB, Huber R, Hausinger RP (2001) Crystal structure of Klebsiella aerogenes UreE, a nickel-binding metallochaperone for urease activation. J Biol Chem 276:49359–49364
Song L, Zhang Y, Chen W, Gu T, Zhang S-Y, Ji Q (2018) Mechanistic insights into staphylopine-mediated metal acquisition. Proc Natl Acad Sci U S A 115:3942–3947
Soriano A, Hausinger RP (1999) GTP-dependent activation of urease apoprotein in complex with the UreD, UreF, and UreG accessory proteins. Proc Natl Acad Sci U S A 96:11140–11144
Soriano A, Colpas GJ, Hausinger RP (2000) UreE stimulation of GTP-dependent urease activation in the UreD-UreF-UreG-urease apoprotein complex. Biochemistry 39:12435–12440
Stähler FN, Odenbreit S, Haas R, Wilrich J, Van Vliet AH, Kusters JG, Kist M, Bereswill S (2006) The novel Helicobacter pylori CznABC metal efflux pump is required for cadmium, zinc, and nickel resistance, urease modulation, and gastric colonization. Infect Immun 74:3845–3852
Stoof J, Kuipers EJ, Klaver G, van Vliet AH (2010a) An ABC transporter and a TonB ortholog contribute to Helicobacter mustelae nickel and cobalt acquisition. Infect Immun 78:4261–4267
Stoof J, Kuipers EJ, van Vliet AHM (2010b) Characterization of NikR-responsive promoters of urease and metal transport genes of Helicobacter mustelae. Biometals 23:145–159
Su C-C, Long F, Zimmermann MT, Rajashankar KR, Jernigan RL, Yu EW (2011) Crystal structure of the CusBA heavy-metal efflux complex of Escherichia coli. Nature 470:558–562
Sukdeo N, Clugston SL, Daub E, Honek JF (2004) Distinct classes of glyoxylase I: metal specificity of the Yersinia pestis, Pseudomonas aeruginosa and Neisseria meningitidis enzymes. Biochem J 384:111–117
Sumner JB (1926) The isolation and crystallization of the enzyme urease. J Biol Chem 69:435–441
Suttisansanee U, Honek JF (2019) Preliminary characterization of a Ni2+-activated and mycothiol-dependent glyoxalase I enzyme from Streptomyces coelicolor. Inorganics 7:99
Suttisansanee U, Lau K, Lagishetty S, Rao KN, Swaminathan S, Sauder JM, Burley SK, Honek JF (2011) Structural variation in bacterial glyoxylase I enzymes. Investigation of the metalloenzyme glyoxalase I from Clostridium acetobutylicum. J Biol Chem 286:38367–38374
Svetlitchnyi V, Dobbek H, Meyer-Klaucke W, Meins T, Thiele B, Römer P, Huber R, Meyer O (2004) A functional Ni-Ni-[4Fe-4S] cluster in the monomeric acetyl-CoA synthase from Carboxydothermus hydrogenoformans. Proc Natl Acad Sci U S A 101:446–451
Symmonds MF, Marshall RL, Bavro VN (2015) Architecture and roles of periplasmic adaptor proteins in tripartite efflux assemblies. Front Microbiol 6:513
Takeuchi T (1909) On the occurrence of urease in higher plants. J Coll Agric Imp Univ Tokyo i:1
Tamagnini P, Leitao E, Oliveira P, Ferreira D, Pinto F, Harris DJ, Heidorn T, Lindblad P (2007) Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol Rev 31:692–720
Tatum EL, Peterson WH, Fred EB (1936) CCLXVI. Enzymic racemization of optically active lactic acid. Biochem J 30:1892–1897
Taylor CD, Wolfe RS (1974) Structure and methylation of coenzyme M (HSCH2CH2SO3). J Biol Chem 249:4879–4885
Techtmann SM, Lebedinsky AV, Colman AS, Sokolova TG, Woyke T, Goodwin L, Robb FT (2012) Evidence for horizontal gene transfer of anaeobic carbon monoxide dehydrogenases. Front Microbiol 3:132
Terlesky KC, Nelson MJ, Ferry JG (1986) Isolation of an enzyme complex with carbon monoxide dehydrogenase activity containing corrinoid and nickel from acetate-grown Methanosarcina thermophila. J Bacteriol 168:1053–1058
Thauer RK (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology 144:2377–2406
Thauer RK (2019) Methyl (alkyl)-coenzyme M reductases: nickel F-430-containing enzymes involved in anaerobic methane formation and in anaerobic oxidation of methane or of short chain alkanes. Biochemistry 58:5198–5220
Thauer RK, Bonacker LG (1994) Biosynthesis of coenzyme F430, a nickel porphinoid involved in methanogenesis. Ciba Found Symp 180:210–227
Thauer RK, Kaster A-K, Goenrich M, Schick M, Hiromoto T, Shima S (2010) Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annu Rev Biochem 79:507–536
Tian J, Wu N, Li J, Liu Y, Guo J, Yao B, Fan Y (2007) Nickel-resistant determinant from Leptospirillum ferriphilum. Appl Environ Microbiol 73:2364–2368
Tibazarwa C, Wuertz S, Mergeay M, Wyns L, van der Lelie D (2000) Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J Bacteriol 182:1399–1409
Timm J, Brochier-Armanet C, Perard J, Zambelli B, Ollganier-de-Choudens S, Ciurli S, Cavazza C (2017) The CO dehydrogenase accessory protein CooT is a novel nickel-binding protein. Metallomics 9:575–583
Tominaga T, Watanabe S, Matsumi R, Atomi H, Imanaka T, Miki K (2012) Structure of the [NiFe]-hydrogenase maturation protein HypF from Thermococcus kodakarensis. Acta Crystallogr F68:1153–1157
Tominaga T, Watanabe S, Matsumi R, Atomi H, Imanaka T, Miki K (2013) Crystal structures of the carbamoylated and cyanated forms of HypE for [NiFe] hydrogenase maturation. Proc Natl Acad Sci U S A 110:20485–20490
Trepreau J, de Rosny E, Duboc C, Sarret G, Petit-Hartlein I, Maillard AP, Imberty A, Proux O, Covès J (2011a) Spectroscopic characterization of the metal-binding sites in the periplasmic metal-sensor domain of CnrX from Cupriavidus metallidurans CH34. Biochemistry 50:9036–9045
Trepreau J, Girard E, Maillard AP, de Rosny E, Petit-Hartlein I, Kahn R, Covès J (2011b) Structural basis for metal sensing by CnrX. J Mol Biol 408:766–779
Tripathi VN, Srivastava S (2006) Extracytoplasmid storage as the nickel resistance mechanism in a natural isolate of Pseudomonas putida S4. Can J Microbiol 52:287–292
Tsang KL, Wong KB (2022) Moving nickel along the hydrogenase-urease maturation pathway. Metallomics. https://doi.org/10.1093/mtomcs/mfac003
Turmo A, Hu J, Hausinger RP (2022) Characterization of the nickel-inserting cyclometallase LarC from Moorella thermoacetica and identification of a CMPylated reaction intermediate. Metallomics. https://doi.org/10.1093/mtomcs/mfac014
Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208
Van der Linden P, Burgdorf T, Bernhard M, Belijlevens B, Friedrich B, Albracht SPJ (2004) The soluble [NiFe]-hydrogenase from Ralstonia eutropha contains four cyanides in its active site, one of which is responsible for the insensitivity towards oxygen. J Biol Inorg Chem 9:616–626
Van Nostrand JD, Arthur JM, Kilpatrick LE, Neely BA, Bertsch PM, Morris PJ (2008) Changes in protein expression in Burkholderia vietnamiensis PR1 301 at pH 5 and 7 with and without nickel. Microbiology 154:3813–3824
van Tieghem PEL (1984) Recherches sur la fermentation de l’urée. C R Acad Sci 58:40
van Vliet AHM, Poppelaars SW, Davies BJ, Stoof J, Bereswill S, Kist M, Penn CW, Kuipers EJ, Kusters JG (2002) NikR mediates nickel-responsive transcriptional induction of urease expression in Helicobacter pylori. Infect Immun 70:2846–2852
van Vliet AHM, Ernst FD, Kusters JG (2004) NikR-mediated regulation of Helicobacter pylori acid adaptation. Trends Microbiol 12:489–494
Vannini A, Pinatel E, Constantini PE, Roncarati D, Puccio S, De Bellis G, Peano C, Danielli A (2017) Comprehensive mapping of the Helicobacter pylori NikR regulon provides new insights in bacterial responses. Sci Rep 7:45458
Vickers TJ, Greig N, Fairlamb AH (2004) A trypanothione-dependent glyoxalase I with a prokaryotic ancestry in Leishmania major. Proc Natl Acad Sci U S A 101:13186–13191
Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272
Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501
Vinella D, Fischer F, Vorontsov E, Gallaud J, Malosse C, Michel V, Cavazza C, Robbe-Saule M, Richaud P, Chamot-Rooke J, Brochier-Armanet C, De Reuse H (2015) Evolution of Helicobacter: acquisition by gastric species of two histidine-rich proteins essential for colonization. PLoS Pathog 11:e1005312
Vitt S, Ma K, Warkentin E, Moll J, Pierik AJ, Shima S, Ermler U (2014) The F420-reducing [NiFe]-hydrogenase complex from Methanothermobacter marburgensis, the first X-ray structure of a group 3 family member. J Mol Biol 426:2813–2826
Volbeda A, Fontecilla-Camps JC (2017) Crystallographic analyses of the active site chemistry and oxygen sensitivity of [NiFe(Se)]-hydrogenases. In: Zamble D, Rowinska-Zyrek M, Kozlowski H (eds) The biological chemistry of nickel. Royal Society of Chemistry, London
Volbeda A, Charon M-H, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373:580–587
Volbeda A, Garcin E, Piras C, de Lacey AL, Fernandez VM, Hatchikian EC, Frey M, Fontecilla-Camps JC (1996) Structure of the [NiFe] hydrogenase active site: evidence for biologically uncommon Fe ligands. J Am Chem Soc 118:12989–12996
Volbeda A, Martin L, Cavazza C, Matho M, Faber BW, Rosebloom W, Albracht SPJ, Garcia E, Rousset M, Fontecilla-Camps JC (2005) Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J Biol Inorg Chem 10:239–249
Volbeda A, Amara P, Darnault C, Mouesca J-M, Parkin A, Roessler MM, Armstrong FA, Fontecilla-Camps JC (2012) X-ray crystallographic and computational studies of the O2-tolerant [NiFe]-hydrogenase 1 from Escherichia coli. Proc Natl Acad Sci U S A 109:5305–5310
Volbeda A, Darnault C, Parkin A, Sargent F, Armstrong FA, Fontecilla-Camps JC (2013) Crystal structure of the O2-tolerant membrane-bound hydrogenase 1 from Escherichia coli in complex with its cognate cytochrome b. Structure 21:184–190
Voordouw G (2002) Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough. J Bacteriol 184:5903–5911
Wang WC, Hsu WH, Chien FT, Chen CY (2001) Crystal structure and site-directed mutagenesis studies of N-carbamoyl-D-amino-acid amidohydrolase from Agrobacterium radiobacter reveals a homotetramer and insight into a catalytic cleft. J Mol Biol 306:251–261
Wang SC, Dias AV, Bloom SL, Zamble DB (2004) The selectivity of metal binding and the metal-induced stability of Escherichia coli NikR. Biochemistry 43:10018–10028
Wang SC, Li Y, Ho MY, Bernal M-E, Sydor AM, Kagzi WR, Zamble DB (2010a) The response of Escherichia coli NikR to nickel: a second nickel-binding site. Biochemistry 49:6635–6645
Wang SC, Li Y, Robinson CV, Zamble DB (2010b) Potassium is critical for the Ni(II)-responsive DNA-binding activity of Escherichia coli NikR. J Am Chem Soc 132:1506–1507
Wang S, Wu Y, Outten FW (2011) Fur and the novel regulator YqjI control transcription of the ferric reductase gene yqjH in Escherichia coli. J Bacteriol 193:563–574
Wang S, Blahut M, Wu Y, Philipkosky KE, Outten FW (2014) Communication between binding sites is required for YqjI regulation of target promoters within the yqjH-yqjI intergenic region. J Bacteriol 196:3199–3207
Wang Y, Branicky R, Noë A, Hekimi S (2018) Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling. J Cell Biol 217:1915–1928
Wang Y, Wegener G, Hou J, Wang J, Xiao X (2019) Expanding anaerobic alkane metabolism in the domain of archaea. Nat Microbiol 4:595–602
Wang Y, Wegener G, Ruff SE, Wang F (2020) Methyl/alkyl-coenzyme M reductase-based anaerobic alkane oxidation in archae. Environ Microbiol 23:530–541
Watanabe S, Matsumi R, Arai T, Atomi H, Imanaka T, Miki K (2007) Crystal structures of [NiFe] hydrogenase maturation proteins HypC, HypD, and HypE: insights into cyanation reaction by thiol redox signaling. Mol Cell 27:29–40
Watanabe S, Arai T, Matsumi R, Atomi H, Imanaka T, Miki K (2009) Crystal structure of HypA, a nickel-binding metallochaperone for [NiFe] hydrogenase maturation. J Mol Biol 394:448–459
Watanabe S, Matsumi R, Atomi H, Imanaka T, Miki K (2012) Crystal structures of the HypCD complex and the HypCDE ternary complex: transient intermediate complexes during [NiFe] hydrogenase maturation. Structure 20:2124–2137
Watanabe S, Kawashima T, Nishitani Y, Kanai T, Wada T, Inaba K, Atomi H, Imanaka T, Miki K (2015) Structural basis of a Ni acquisition cycle for [NiFe] hydrogenase by Ni-metallochaperone HypA and its enhancer. Proc Natl Acad Sci U S A 112:7701–7706
Watt RK, Ludden PW (1998) The identification, purification, and characterization of CooJ. A nickel-binding protein that is co-regulated with the Ni-containing CO dehydrogenase from Rhodospirillum rubrum. J Biol Chem 273:10019–10025
Weeks DL, Eskandar S, Scott DR, Sachs G (2000) A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287:482–485
Weimer PJ, Moen GN (2013) Quantitative analysis of growth and volatile fatty acid production by the anaerobic ruminal bacterium Megasphaera elsdenii T81. Appl Microbiol Biotechnol 97:4075–4081
West AL, St John F, Lopes PEM, MacKerell AD Jr, Pozharski E, Michel SLJ (2010) Holo-Ni(II)HpNikR is an asymmetric tetramer containing two different nickel-binding sites. J Am Chem Soc 132:14447–14456
Willecke K, Gries E-M, Oehr P (1973) Coupled transport of citrate and magnesium in Bacillus subtilis. J Bacteriol 218:807–814
Wittenborn EC, Merrouch M, Ueda C, Fradale L, Léger C, Fourmond V, Pandelia M-E, Dementin S, Drennan CL (2018) Redoxdependent rearrangements of the NiFeS cluster of carbon monoxide dehydrogenase elife 7:e39451
Wittenborn EC, Cohen SE, Merrouch M, Léger C, Fourmond V, Dementin S, Drennan CL (2019) Structural insight into the metallocofactor maturation in carbon monoxide dehydrogenase. J Biol Chem 294:13017–13026
Wittenborn EC, Guendon C, Merrouch M, Benvenuti M, Fourmond V, Léger C, Drennan CL, Dementin S (2020) The solvent-exposed Fe-S D-cluster contributes to oxygen-resistance in Desulfovibrio vulgaris Ni-Fe carbon monoxide dehydrogenase. ACS Catal 10:7328–7335
Wöhler F (1828) Ueber künstliche bildung des harnstoffs (On the artificial formation of urea). Annalen der Physik (Berlin) 12:253–256
Wolfram L, Bauerfeind P (2002) Conserved low-affinity nickel-binding amino acids are essential for the function of the nickel permease NixA of Helicobacter pylori. J Bacteriol 184:1438–1443
Wolfram L, Haas E, Bauerfeind P (2006) Nickel represses the synthesis of the nickel permease NixA of Helicobacter pylori. J Bacteriol 188:1245–1250
Wray JW, Abeles RH (1993) A bacterial enzyme that catalyzes formation of carbon monoxide. J Biol Chem 268:21466–21469
Wroblewski LE, Peek RM Jr, Wilson KT (2010) Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 23:713–739
Wu M, Ren Q, Durkin AS, Daugherty SC, Brinkac LM, Dodson RJ, Madupu R, Sullivan SA, Kolonay JF, Haft DH, Nelson WC, Tallon LJ, Jones KM, Ulrich LE, Gonzalez JM, Zhulin IB, Robb FT, Eisen JA (2005) Life in hot carbon monoxide: the complete genome sequence of Carboxydothermus hydrogenoformans Z-2901. PLoS Genet 1:e65
Wuerges J, Lee J-W, Yim Y-I, Kang SO, Carugo KD (2004) Crystal structure of nickel-containing superoxide dismutase reveals another type of active site. Proc Natl Acad Sci U S A 101:8569–8574
Wülfing C, Lombardero J, Plückthun A (1994) An Escherichia coli protein consisting of a domain homologous to FK506-binding proteins (FKBP) and a new metal binding motif. J Biol Chem 269:2895–2901
Xu J, Cotruvo JA Jr (2020) The czcD (NiCo) riboswitch responds to iron(II). Biochemistry 59:1508–1516
Yang F, Hu W, Xu H, Li C, Xia B, Jin C (2006) Structure and backbone dynamics of an endopeptidase HycI from Escherichia coli: implications for mechanism of the [NiFe] hydrogenase maturation. J Biol Chem 282:3856–3863
Yang X, Li H, Cheng T, Xia W, Lai Y-T, Sun H (2014) Nickel translocation between metallochaperones HypA and UreE in Helicobacter pylori. Metallomics 6:1731–1736
Yang X, Li H, Lai T-P, Sun H (2015) UreE-UreG complex facilitates nickel transfer and preactivates GTPase of UreG in Helicobacter pylori. J Biol Chem 290:12474–12485
Youn H-D, Kim E-J, Roe J-H, Hah YC, Kang S-O (1996a) A novel nickel-containing superoxide dismutase from Streptomyces spp. Biochem J 318:889–896
Youn H-D, Youn H, Lee J-W, Yim Y-I, Lee JK, Hah YC, Kang S-O (1996b) Unique isoenzymes of superoxide dismutase in Streptomyces griseus. Arch Biochem Biophys 334:341–348
Yu Y, Zhou M, Kirsch F, Xu C, Zhang L, Wang Y, Jiang Z, Wang N, Li J, Eitinger T, Yang M (2014) Planar substrate-binding site dictates the specificity of ECF-type nickel/cobalt transporters. Cell Res 24:267–277
Yuen MH, Fong YH, Nim YS, Lau PH, Wong K-B (2017) Structural insights into how GTP-dependent conformational changes in a metallochaperone UreG facilitate urease maturation. Proc Natl Acad Sci U S A 114:E10890–E10898
Zadvornyy OA, Allen M, Brumfield SK, Varpness Z, Boyd ES, Zorin NA, Serebriakova L, Douglas T, Peters JW (2010) Hydrogen enhances nickel tolerance in the purple sulfur bacterium Thiocapsa roseopersicina. Environ Sci Technol 44:834–840
Zambelli B, Stola M, Musiani F, De Vriendt K, Samyn B, Devreese B, Van Beeumen J, Dikiy A, Bryant DA, Ciurli S (2005) UreG, a chaperone in the urease assembly process, is an intrinsically unstructured GTPase that specifically binds Zn2+. J Biol Chem 280:4684–4695
Zambelli B, Bellucci M, Danielli A, Scarlato V, Ciurli S (2007a) The Ni2+ binding properties of Helicobacter pylori NikR. Chem Commun 3649–3651
Zambelli B, Musiani F, Savini M, Tucker P, Ciurli S (2007b) Biochemical studies on Mycobacterium tuberculosis UreG and comparative modeling reveal structural and functional conservation among the bacterial UreG family. Biochemistry 46:3171–3182
Zambelli B, Turano P, Musiani F, Neyroz P, Ciurli S (2009) Zn2+-linked dimerization of UreG from Helicobacter pylori, a chaperone involved in nickel trafficking and urease activation. Proteins 74:222–239
Zambelli B, Cremades N, Neyroz P, Turano P, Uversky VN, Ciurli S (2012) Insights in the (un)structural organization of Bacillus pasteurii UreG, an intrinsically disordered GTPase enzyme. Mol BioSyst 8:220–228
Zambelli B, Banaszak K, Merloni A, Kiliszek A, Rypniewski W, Ciurli S (2013) Selectivity of Ni(II) and Zn(II) binding to Sporosarcina pasteurii UreE, a metallochaperone in the urease assembly: a calorimetric and crystallographic study. J Biol Inorg Chem 18:1005–1017
Zamble D, Rowinska-Zyrek M, Kozlowski H (2017) The biological chemistry of nickel. Royal Society of Chemistry, Cambridge
Zeer-Wanklyn CJ, Zamble DB (2017) Microbial nickel: cellular uptake and delivery to enzyme centers. Curr Opin Chem Biol 37:80–88
Zeng Y-B, Zhang D-M, Li H, Sun H (2008) Binding of Ni2+ to a histidine- and glutamine-rich protein, Hpn-like. J Biol Inorg Chem 13:1121–1131
Zeng Y-B, Yang N, Sun H (2011) Metal-binding properties of an Hpn-like histidine-rich protein. Chem Eur J 17:5852–5860
Zhan G, Li D, Zhang L (2012) Aerobic bioreduction of nickel(II) to elemental nickel with concomitant biomineralization. Appl Microbiol Biotechnol 96:273–281
Zhang JW, Butland G, Greenblatt JF, Emili A, Zamble DB (2005) A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway. J Biol Chem 280:4360–4366
Zhu T, Tian J, Zhang S, Wu N, Fan Y (2011) Identification of the transcriptional regulator NcrB in the nickel resistance determinant of Leptospirillum ferriphilum UBK03. PLoS One 6:e17367
Ziani W, Maillard AP, Petit-Hartlein I, Garnier N, Crouzy S, Girard E, Covès J (2014) The X-ray structure of NccX from Cupriavidus metallidurans 31A illustrates potential dangers of detergent solubilization when generating and interpreting crystal structures of membrane proteins. J Biol Chem 289:31160–31172
Zielazinski EL, Gonzalez-Guerrero M, Subramanian P, Stemmler TL, Argüello JM, Rosenzweig AC (2013) Sinorhizobium meliloti Nia is a P-ATPase expressed in the nodule during plant symbiosis and is involved in Ni and Fe transport. Metallomics 5:1614–1623
Acknowledgements
Experimental investigations of microbial nickel metabolism in the Hausinger lab are supported by the National Institutes of Health (GM128959) and the National Science Foundation (CHE-1807073). I thank the many colleagues of my laboratory who have contributed to this work over the years.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Hausinger, R.P. (2022). Microbial Metabolism of Nickel. In: Hurst, C.J. (eds) Microbial Metabolism of Metals and Metalloids. Advances in Environmental Microbiology, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-030-97185-4_14
Download citation
DOI: https://doi.org/10.1007/978-3-030-97185-4_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-97184-7
Online ISBN: 978-3-030-97185-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)