Abstract
Iron is essential to nearly all forms of life, but the redox activity of this element necessitates its cellular regulation. All iron-utilizing organisms require this nutrient to be tightly managed, which is accomplished by a suite of proteins and nucleic acids involved in the acquisition, the delivery, the storage, the regulation, and the export of this essential element. For infectious organisms, iron acquisition systems are commonly associated with intracellular growth, survival, and virulence of pathogens, which are dynamically able to modify their iron uptake strategies in response to changing host environments. The past few decades have been marked with an increased understanding of pathogenic ferric iron (Fe3+) and heme acquisition. In contrast, though the necessity of ferrous iron (Fe2+) transport for pathogenesis has been established, the precise details of this process remain enigmatic, and Fe2+ transporters remain unexploited as drug targets to combat drug-resistant organisms. This chapter will overview a current understanding of Fe2+ transport in microbes and highlight gaps in our knowledge that must be closed in order to establish a comprehensive understanding of unicellular Fe2+ metabolism.
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References
Abeyrathna SS, Abeyrathna NS, Thai NK, Sarkar P, D’Arcy S, Meloni G (2019) IroT/MavN is a Legionella transmembrane Fe(II) transporter: metal selectivity and translocation kinetics revealed by in vitro real-time transport. Biochemistry 58(43):4337–4342. https://doi.org/10.1021/acs.biochem.9b00658
Abu Kwaik Y, Bumann D (2013) Microbial quest for food in vivo: ‘nutritional virulence’ as an emerging paradigm. Cell Microbiol 15(6):882–890. https://doi.org/10.1111/cmi.12138
Álvarez-Fraga L, Vázquez-Ucha JC, Martínez-Guitián M, Vallejo JA, Bou G, Beceiro A, Poza M (2018) Pneumonia infection in mice reveals the involvement of the feoA gene in the pathogenesis of Acinetobacter baumannii. Virulence 9(1):496–509. https://doi.org/10.1080/21505594.2017.1420451
Andrews SC, Robinson AK, Rodríguez-Quiñones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27(2-3):215–237
Antibiotic resistance threats in the United States (2019)
Aranda J, Cortés P, Garrido ME, Fittipaldi N, Llagostera M, Gottschalk M, Barbé J (2009) Contribution of the FeoB transporter to Streptococcus suis virulence. Int Microbiol 12(2):137–143
Ash MR, Maher MJ, Guss JM, Jormakka M (2011) The initiation of GTP hydrolysis by the G-domain of FeoB: insights from a transition-state complex structure. PLoS One 6(8):e23355. https://doi.org/10.1371/journal.pone.0023355
Askwith C, Kaplan J (1997) An oxidase-permease-based iron transport system in Schizosaccharomyces pombe and its expression in Saccharomyces cerevisiae. J Biol Chem 272(1):401–405. https://doi.org/10.1074/jbc.272.1.401
Askwith C, Eide D, Van Ho A, Bernard PS, Li L, Davis-Kaplan S, Sipe DM, Kaplan J (1994) The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76(2):403–410. https://doi.org/10.1016/0092-8674(94)90346-8
Bazylinski DA, Frankel RB, Jannasch HW (1988) Anaerobic magnetite production by a marine, magnetotactic bacterium. Nature 334(6182):518–519. https://doi.org/10.1038/334518a0
Bearden SW, Staggs TM, Perry RD (1998) An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J Bacteriol 180(5):1135–1147
Bennett BD, Brutinel ED, Gralnick JA (2015) A ferrous iron exporter mediates iron resistance in Shewanella oneidensis MR-1. Appl Environ Microbiol 81(22):7938–7944. https://doi.org/10.1128/AEM.02835-15
Bennett BD, Redford KE, Gralnick JA (2018) MgtE homolog FicI acts as a secondary ferrous iron importer in Shewanella oneidensis strain MR-1. Appl Environ Microbiol 84(6). https://doi.org/10.1128/AEM.01245-17
Bhattacharyya P (1970) Active transport of manganese in isolated membranes of Escherichia coli. J Bacteriol 104(3):1307–1311. https://doi.org/10.1128/JB.104.3.1307-1311.1970
Blakemore R (1975) Magnetotactic bacteria. Science 190(4212):377–379. https://doi.org/10.1126/science.170679
Bos JL, Rehmann H, Wittinghofer A (2007) GEFs and GAPs: critical elements in the control of small G proteins. Cell 129(5):865–877. https://doi.org/10.1016/j.cell.2007.05.018
Bozzi AT, Bane LB, Weihofen WA, Singharoy A, Guillen ER, Ploegh HL, Schulten K, Gaudet R (2016) Crystal structure and conformational change mechanism of a bacterial Nramp-family divalent metal transporter. Structure 24(12):2102–2114. https://doi.org/10.1016/j.str.2016.09.017
Brunori M (2010) Myoglobin strikes back. Protein Sci 19(2):195–201. https://doi.org/10.1002/pro.300
Brutinel ED, Gralnick JA (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biotechnol 93(1):41–48. https://doi.org/10.1007/s00253-011-3653-0
Caccavo F, Lonergan DJ, Lovley DR, Davis M, Stolz JF, McInerney MJ (1994) Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol 60(10):3752–3759. https://doi.org/10.1128/AEM.60.10.3752-3759.1994
Cain TJ, Smith AT (2021) Ferric iron reductases and their contribution to unicellular ferrous iron uptake. J Inorg Biochem 218:111407. https://doi.org/10.1016/j.jinorgbio.2021.111407
Calugay RJ, Miyashita H, Okamura Y, Matsunaga T (2003) Siderophore production by the magnetic bacterium Magnetospirillum magneticum AMB-1. FEMS Microbiol Lett 218(2):371–375. https://doi.org/10.1016/S0378-1097(02)01188-6
Calugay RJ, Takeyama H, Mukoyama D, Fukuda Y, Suzuki T, Kanoh K, Matsunaga T (2006) Catechol siderophore excretion by magnetotactic bacterium Magnetospirillum magneticum AMB-1. J Biosci Bioeng 101(5):445–447. https://doi.org/10.1263/jbb.101.445
Cao J, Woodhall MR, Alvarez J, Cartron ML, Andrews SC (2007) EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol Microbiol 65(4):857–875. https://doi.org/10.1111/j.1365-2958.2007.05802.x
Carlson HK, Clark IC, Melnyk RA, Coates JD (2012) Toward a mechanistic understanding of anaerobic nitrate-dependent iron oxidation: balancing electron uptake and detoxification. Front Microbiol 3:57. https://doi.org/10.3389/fmicb.2012.00057
Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo-transport of ferrous iron into bacteria. Biometals 19(2):143–157. https://doi.org/10.1007/s10534-006-0003-2
Chao Y, Fu D (2004) Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J Biol Chem 279(17):17173–17180. https://doi.org/10.1074/jbc.M400208200
Christenson ET, Isaac DT, Yoshida K, Lipo E, Kim JS, Ghirlando R, Isberg RR, Banerjee A (2019) The iron-regulated vacuolar. Proc Natl Acad Sci U S A 116(36):17775–17785. https://doi.org/10.1073/pnas.1902806116
Chu BC, Garcia-Herrero A, Johanson TH, Krewulak KD, Lau CK, Peacock RS, Slavinskaya Z, Vogel HJ (2010) Siderophore uptake in bacteria and the battle for iron with the host; a bird’s eye view. Biometals 23(4):601–611. https://doi.org/10.1007/s10534-010-9361-x
Cornelis P (2010) Iron uptake and metabolism in pseudomonads. Appl Microbiol Biotechnol 86(6):1637–1645. https://doi.org/10.1007/s00253-010-2550-2
Coudray N, Valvo S, Hu M, Lasala R, Kim C, Vink M, Zhou M, Provasi D, Filizola M, Tao J, Fang J, Penczek PA, Ubarretxena-Belandia I, Stokes DL (2013) Inward-facing conformation of the zinc transporter YiiP revealed by cryoelectron microscopy. Proc Natl Acad Sci U S A 110(6):2140–2145. https://doi.org/10.1073/pnas.1215455110
Crack JC, Le Brun NE, Thomson AJ, Green J, Jervis AJ (2008) Reactions of nitric oxide and oxygen with the regulator of fumarate and nitrate reduction, a global transcriptional regulator, during anaerobic growth of Escherichia coli. Methods Enzymol 437:191–209. https://doi.org/10.1016/S0076-6879(07)37011-0
D’Aquino JA, Ringe D (2003) Determinants of the SRC homology domain 3-like fold. J Bacteriol 185(14):4081–4086. https://doi.org/10.1128/jb.185.14.4081-4086.2003
Dashper SG, Butler CA, Lissel JP, Paolini RA, Hoffmann B, Veith PD, O’Brien-Simpson NM, Snelgrove SL, Tsiros JT, Reynolds EC (2005) A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J Biol Chem 280(30):28095–28102. https://doi.org/10.1074/jbc.M503896200
DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Syst Biol 50(4):470–478
Derry LA (2015) Causes and consequences of mid-Proterozoic anoxia. Geophys Res Lett 42(20):8538–8546. https://doi.org/10.1002/2015GL065333
Deshpande CN, McGrath AP, Font J, Guilfoyle AP, Maher MJ, Jormakka M (2013) Structure of an atypical FeoB G-domain reveals a putative domain-swapped dimer. Acta Crystallogr Sect F Struct Biol Cryst Commun 69(4):399–404. https://doi.org/10.1107/S1744309113005939
Dong Z, Guo S, Fu H, Gao H (2017) Investigation of a spontaneous mutant reveals novel features of iron uptake in Shewanella oneidensis. Sci Rep 7(1):11788. https://doi.org/10.1038/s41598-017-11987-3
Dunning JC, Ma Y, Marquis RE (1998) Anaerobic killing of oral streptococci by reduced, transition metal cations. Appl Environ Microbiol 64(1):27–33. https://doi.org/10.1128/AEM.64.1.27-33.1998
Ehrnstorfer IA, Geertsma ER, Pardon E, Steyaert J, Dutzler R (2014) Crystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transport. Nat Struct Mol Biol 21(11):990–996. https://doi.org/10.1038/nsmb.2904
Ellermann M, Arthur JC (2017) Siderophore-mediated iron acquisition and modulation of host-bacterial interactions. Free Radic Biol Med 105:68–78. https://doi.org/10.1016/j.freeradbiomed.2016.10.489
Embree M, Qiu Y, Shieu W, Nagarajan H, O’Neil R, Lovley D, Zengler K (2014) The iron stimulon and fur regulon of Geobacter sulfurreducens and their role in energy metabolism. Appl Environ Microbiol 80(9):2918–2927. https://doi.org/10.1128/AEM.03916-13
Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583. https://doi.org/10.1146/annurev.micro.112408.134208
Emerson D, Scott JJ, Benes J, Bowden WB (2015) Microbial iron oxidation in the Arctic tundra and its implications for biogeochemical cycling. Appl Environ Microbiol 81(23):8066–8075. https://doi.org/10.1128/AEM.02832-15
Eng ET, Jalilian AR, Spasov KA, Unger VM (2008) Characterization of a novel prokaryotic GDP dissociation inhibitor domain from the G protein coupled membrane protein FeoB. J Mol Biol 375(4):1086–1097. https://doi.org/10.1016/j.jmb.2007.11.027
Escolar L, Pérez-Martín J, de Lorenzo V (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181(20):6223–6229
Esther J, Sukla LB, Pradhan N, Panda S (2015) Fe (III) reduction strategies of dissimilatory iron reducing bacteria. Korean J Chem Eng 32(1):1–14. https://doi.org/10.1007/s11814-014-0286-x
Fillat MF (2014) The FUR (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators. Arch Biochem Biophys 546:41–52. https://doi.org/10.1016/j.abb.2014.01.029
Fischbach MA, Lin H, Liu DR, Walsh CT (2006) How pathogenic bacteria evade mammalian sabotage in the battle for iron. Nat Chem Biol 2(3):132–138. https://doi.org/10.1038/nchembio771
Ganz T (2008) Iron homeostasis: fitting the puzzle pieces together. Cell Metab 7(4):288–290. https://doi.org/10.1016/j.cmet.2008.03.008
Gauger T, Konhauser K, Kappler A (2015) Protection of phototrophic iron(II)-oxidizing bacteria from UV irradiation by biogenic iron(III) minerals: implications for early Archean banded iron formation. Geology 43(12):1067–1070. https://doi.org/10.1130/G37095.1
Gauger T, Konhauser K, Kappler A (2016) Protection of nitrate-reducing Fe(II)-oxidizing bacteria from UV radiation by biogenic Fe(III) minerals. Astrobiology 16(4):301–310. https://doi.org/10.1089/ast.2015.1365
Glass J (2015) Microbes that meddle with metals: microorganisms depend on numerous metal cofactors; these requirements in turn depend on microbial species, type of metabolism, and environmental conditions. Microbe 10:197–202. https://doi.org/10.1128/microbe.10.197.1
Grass G, Wong MD, Rosen BP, Smith RL, Rensing C (2002) ZupT is a Zn(II) uptake system in Escherichia coli. J Bacteriol 184(3):864–866. https://doi.org/10.1128/jb.184.3.864-866.2002
Grass G, Franke S, Taudte N, Nies DH, Kucharski LM, Maguire ME, Rensing C (2005a) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187(5):1604–1611. https://doi.org/10.1128/JB.187.5.1604-1611.2005
Grass G, Otto M, Fricke B, Haney CJ, Rensing C, Nies DH, Munkelt D (2005b) FieF (YiiP) from Escherichia coli mediates decreased cellular accumulation of iron and relieves iron stress. Arch Microbiol 183(1):9–18. https://doi.org/10.1007/s00203-004-0739-4
Grosse C, Scherer J, Koch D, Otto M, Taudte N, Grass G (2006) A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli. Mol Microbiol 62(1):120–131. https://doi.org/10.1111/j.1365-2958.2006.05326.x
Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465(1-2):190–198. https://doi.org/10.1016/s0005-2736(00)00138-3
Guilfoyle AP, Deshpande CN, Schenk G, Maher MJ, Jormakka M (2014) Exploring the correlation between the sequence composition of the nucleotide binding G5 loop of the FeoB GTPase domain (NFeoB) and intrinsic rate of GDP release. Biosci Rep 34(6):e00158. https://doi.org/10.1042/BSR20140152
Hagelueken G, Duthie FG, Florin N, Schubert E, Schiemann O (2015) Expression, purification and spin labelling of the ferrous iron transporter FeoB from Escherichia coli BL21 for EPR studies. Protein Expr Purif 114:30–36. https://doi.org/10.1016/j.pep.2015.05.014
Hagelueken G, Hoffmann J, Schubert E, Duthie FG, Florin N, Konrad L, Imhof D, Behrmann E, Morgner N, Schiemann O (2016) Studies on the X-ray and solution structure of FeoB from Escherichia coli BL21. Biophys J 110(12):2642–2650. https://doi.org/10.1016/j.bpj.2016.05.018
Hanert H (1974) In vivo kinetics of individual development of Gallionella ferruginea in batch microculture. Arch Microbiol 96(1):59–74. https://doi.org/10.1007/BF00590163
Hantke K (1987) Ferrous iron transport mutants in Escherichia coli K12. FEMS Microbiol Lett 44(1):53–57. https://doi.org/10.1111/j.1574-6968.1987.tb02241.x
Hantke K (2003) Is the bacterial ferrous iron transporter FeoB a living fossil? Trends Microbiol 11(5):192–195
Hider RC, Kong X (2013) Iron speciation in the cytosol: an overview. Dalton Trans 42(9):3220–3229. https://doi.org/10.1039/c2dt32149a
Hsueh KL, Yu LK, Chen YH, Cheng YH, Hsieh YC, Ke SC, Hung KW, Chen CJ, Huang TH (2013) FeoC from Klebsiella pneumoniae contains a [4Fe-4S] cluster. J Bacteriol 195(20):4726–4734. https://doi.org/10.1128/jb.00687-13
Hu Y, Ribbe MW (2015) Nitrogenase and homologs. J Biol Inorg Chem 20(2):435–445. https://doi.org/10.1007/s00775-014-1225-3
Huang W, Wilks A (2017) Extracellular heme uptake and the challenge of bacterial cell membranes. Annu Rev Biochem 86:799–823. https://doi.org/10.1146/annurev-biochem-060815-014214
Hung KW, Juan TH, Hsu YL, Huang TH (2012a) NMR structure note: the ferrous iron transport protein C (FeoC) from Klebsiella pneumoniae. J Biomol NMR 53(2):161–165. https://doi.org/10.1007/s10858-012-9633-6
Hung KW, Tsai JY, Juan TH, Hsu YL, Hsiao CD, Huang TH (2012b) Crystal structure of the Klebsiella pneumoniae NFeoB/FeoC complex and roles of FeoC in regulation of Fe2+ transport by the bacterial Feo system. J Bacteriol 194(23):6518–6526. https://doi.org/10.1128/JB.01228-12
Hunter RC, Asfour F, Dingemans J, Osuna BL, Samad T, Malfroot A, Cornelis P, Newman DK (2013) Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways. mBio 4(4). https://doi.org/10.1128/mBio.00557-13
Ikeda JS, Janakiraman A, Kehres DG, Maguire ME, Slauch JM (2005) Transcriptional regulation of sitABCD of Salmonella enterica serovar typhimurium by MntR and Fur. J Bacteriol 187(3):912–922. https://doi.org/10.1128/JB.187.3.912-922.2005
Isaac DT, Laguna RK, Valtz N, Isberg RR (2015) MavN is a Legionella pneumophila vacuole-associated protein required for efficient iron acquisition during intracellular growth. Proc Natl Acad Sci U S A 112(37):E5208–E5217. https://doi.org/10.1073/pnas.1511389112
Janakiraman A, Slauch JM (2000) The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol Microbiol 35(5):1146–1155. https://doi.org/10.1046/j.1365-2958.2000.01783.x
Jones DS, Kohl C, Grettenberger C, Larson LN, Burgos WD, Macaladya JL (2015) Geochemical niches of iron-oxidizing acidophiles in acidic coal mine drainage. Appl Environ Microbiol 81(4):1242–1250. https://doi.org/10.1128/AEM.02919-14
Kadi N, Arbache S, Song L, Oves-Costales D, Challis GL (2008) Identification of a gene cluster that directs putrebactin biosynthesis in Shewanella species: PubC catalyzes cyclodimerization of N-hydroxy-N-succinylputrescine. J Am Chem Soc 130(32):10458–10459. https://doi.org/10.1021/ja8027263
Kammler M, Schön C, Hantke K (1993) Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175(19):6212–6219. https://doi.org/10.1128/jb.175.19.6212-6219.1993
Kehres DG, Zaharik ML, Finlay BB, Maguire ME (2000) The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol 36(5):1085–1100. https://doi.org/10.1046/j.1365-2958.2000.01922.x
Kehres DG, Janakiraman A, Slauch JM, Maguire ME (2002) SitABCD is the alkaline Mn2+ transporter of Salmonella enterica serovar typhimurium. J Bacteriol 184(12):3159. https://doi.org/10.1128/JB.184.12.3159-3166.2002
Kim H, Lee H, Shin D (2012) The FeoA protein is necessary for the FeoB transporter to import ferrous iron. Biochem Biophys Res Commun 423(4):733–738. https://doi.org/10.1016/j.bbrc.2012.06.027
Kim H, Lee H, Shin D (2013) The FeoC protein leads to high cellular levels of the Fe(II) transporter FeoB by preventing FtsH protease regulation of FeoB in Salmonella enterica. J Bacteriol 195(15):3364–3370. https://doi.org/10.1128/jb.00343-13
Kim H, Lee H, Shin D (2015) Lon-mediated proteolysis of the FeoC protein prevents Salmonella enterica from accumulating the Fe(II) transporter FeoB under high-oxygen conditions. J Bacteriol 197(1):92–98. https://doi.org/10.1128/jb.01826-14
Konhauser KO, Planavsky NJ, Hardisty DS, Robbins LJ, Warchola TJ, Haugaard R, Lalonde SV, Partin CA, Oonk PBH, Tsikos H, Lyons TW, Bekker A, Johnson CM (2017) Iron formations: a global record of neoarchaean to palaeoproterozoic environmental history. Earth-Sci Rev 172:140–177. https://doi.org/10.1016/j.earscirev.2017.06.012
Koster S, Kuhlbrandt W, Yildiz O (2009a) Purification, crystallization and preliminary X-ray diffraction analysis of the FeoB G domain from Methanococcus jannaschii. Acta Crystallogr Sect F Struct Biol Cryst Commun 65(Pt 7):684–687. https://doi.org/10.1107/s1744309109019216
Koster S, Wehner M, Herrmann C, Kuhlbrandt W, Yildiz O (2009b) Structure and function of the FeoB G-domain from Methanococcus jannaschii. J Mol Biol 392(2):405–419. https://doi.org/10.1016/j.jmb.2009.07.020
Krewulak KD, Vogel HJ (2008) Structural biology of bacterial iron uptake. Biochim Biophys Acta 1778(9):1781–1804. https://doi.org/10.1016/j.bbamem.2007.07.026
Lau CK, Ishida H, Liu Z, Vogel HJ (2013) Solution structure of Escherichia coli FeoA and its potential role in bacterial ferrous iron transport. J Bacteriol 195(1):46–55. https://doi.org/10.1128/jb.01121-12
Lau CK, Krewulak KD, Vogel HJ (2016) Bacterial ferrous iron transport: the Feo system. FEMS Microbiol Rev 40(2):273–298. https://doi.org/10.1093/femsre/fuv049
Ledyard KM, Butler A (1997) Structure of putrebactin, a new dihydroxamate siderophore produced by Shewanella putrefaciens. J Biol Inorg Chem 2(1):93–97. https://doi.org/10.1007/s007750050110
Létoffé S, Heuck G, Delepelaire P, Lange N, Wandersman C (2009) Bacteria capture iron from heme by keeping tetrapyrrol skeleton intact. Proc Natl Acad Sci U S A 106(28):11719–11724. https://doi.org/10.1073/pnas.0903842106
Li SS (2005) Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem J 390(Pt 3):641–653. https://doi.org/10.1042/bj20050411
Li ZQ, Zhang LC, Xue CJ, Zheng MT, Zhu MT, Robbins LJ, Slack JF, Planavsky NJ, Konhauser KO (2018) Earth’s youngest banded iron formation implies ferruginous conditions in the early Cambrian Ocean. Sci Rep 8(1):9970. https://doi.org/10.1038/s41598-018-28187-2
Linkous RO, Sestok AE, Smith AT (2019) The crystal structure of Klebsiella pneumoniae FeoA reveals a site for protein-protein interactions. Proteins 87(11):897–903. https://doi.org/10.1002/prot.25755
Liu X, Du Q, Wang Z, Zhu D, Huang Y, Li N, Wei T, Xu S, Gu L (2011) Crystal structure and biochemical features of EfeB/YcdB from Escherichia coli O157: ASP235 plays divergent roles in different enzyme-catalyzed processes. J Biol Chem 286(17):14922–14931. https://doi.org/10.1074/jbc.M110.197780
Liu L, Li S, Wang S, Dong Z, Gao H (2018) Complex iron uptake by the Putrebactin-mediated and Feo systems in Shewanella oneidensis. Appl Environ Microbiol 84(20). https://doi.org/10.1128/AEM.01752-18
Lovley DR (1997) Microbial Fe(III) reduction in subsurface environments. FEMS Microbiol Rev 20(3-4):305–313. https://doi.org/10.1111/j.1574-6976.1997.tb00316.x
Lovley DR, Walker DJF (2019) Protein Nanowires. Front Microbiol 10:2078. https://doi.org/10.3389/fmicb.2019.02078
Makui H, Roig E, Cole ST, Helmann JD, Gros P, Cellier MF (2000) Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol 35(5):1065–1078. https://doi.org/10.1046/j.1365-2958.2000.01774.x
Mann S, Sparks N, Frankel R, Bazylinski D, Jannasch H (1990) Biomineralization of ferrimagnetic greigite (Fe3S4) and iron pyrite (FeS2) in a magnetotactic bacterium. Nature 343. https://doi.org/10.1038/343258a0
Marlovits TC, Haase W, Herrmann C, Aller SG, Unger VM (2002) The membrane protein FeoB contains an intramolecular G protein essential for Fe(II) uptake in bacteria. Proc Natl Acad Sci U S A 99(25):16243–16248. https://doi.org/10.1073/pnas.242338299
Marshall B, Stintzi A, Gilmour C, Meyer JM, Poole K (2009) Citrate-mediated iron uptake in Pseudomonas aeruginosa: involvement of the citrate-inducible FecA receptor and the FeoB ferrous iron transporter. Microbiology 155(Pt 1):305–315. https://doi.org/10.1099/mic.0.023531-0
Matsunaga T, Sakaguchi T, Tadakoro F (1991) Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl Microbiol Biotechnol 35(5):651–655. https://doi.org/10.1007/BF00169632
Naikare H, Palyada K, Panciera R, Marlow D, Stintzi A (2006) Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect Immun 74(10):5433–5444. https://doi.org/10.1128/iai.00052-06
Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14(2):186–199. https://doi.org/10.1007/BF01569902
Ovchinnikov S, Park H, Varghese N, Huang PS, Pavlopoulos GA, Kim DE, Kamisetty H, Kyrpides NC, Baker D (2017) Protein structure determination using metagenome sequence data. Science (New York, NY) 355(6322):294–298. https://doi.org/10.1126/science.aah4043
Pandey A, Sonti RV (2010) Role of the FeoB protein and siderophore in promoting virulence of Xanthomonas oryzae pv. oryzae on rice. J Bacteriol 192(12):3187–3203. https://doi.org/10.1128/jb.01558-09
Parrow NL, Fleming RE, Minnick MF (2013) Sequestration and scavenging of iron in infection. Infect Immun 81(10):3503–3514
Patzer SI, Hantke K (2001) Dual repression by Fe2+-Fur and Mn2+-MntR of the mntH gene, encoding an NRAMP-like Mn2+ transporter in Escherichia coli. J Bacteriol 183(16):4806–4813. https://doi.org/10.1128/JB.183.16.4806-4813.2001
Paulsen IT, Saier MH (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156(2):99–103. https://doi.org/10.1007/s002329900192
Pérez N, Johnson R, Sen B, Ramakrishnan G (2016) Two parallel pathways for ferric and ferrous iron acquisition support growth and virulence of the intracellular pathogen Francisella tularensis Schu S4. MicrobiologyOpen 5(3):453–468. https://doi.org/10.1002/mbo3.342
Perry RD, Mier I Jr, Fetherston JD (2007) Roles of the Yfe and Feo transporters of Yersinia pestis in iron uptake and intracellular growth. Biometals 20(3-4):699–703. https://doi.org/10.1007/s10534-006-9051-x
Perry RD, Craig SK, Abney J, Bobrov AG, Kirillina O, Mier I, Truszczynska H, Fetherston JD (2012) Manganese transporters Yfe and MntH are Fur-regulated and important for the virulence of Yersinia pestis. Microbiology 158(Pt 3):804–815. https://doi.org/10.1099/mic.0.053710-0
Portier E, Zheng H, Sahr T, Burnside DM, Mallama C, Buchrieser C, Cianciotto NP, Héchard Y (2015) IroT/mavN, a new iron-regulated gene involved in Legionella pneumophila virulence against amoebae and macrophages. Environ Microbiol 17(4):1338–1350. https://doi.org/10.1111/1462-2920.12604
Rajasekaran MB, Nilapwar S, Andrews SC, Watson KA (2010) EfeO-cupredoxins: major new members of the cupredoxin superfamily with roles in bacterial iron transport. Biometals 23(1):1–17. https://doi.org/10.1007/s10534-009-9262-z
Raphael BH, Joens LA (2003) FeoB is not required for ferrous iron uptake in Campylobacter jejuni. Can J Microbiol 49(11):727–731. https://doi.org/10.1139/w03-086
Richard KL, Kelley BR, Johnson JG (2019) Heme uptake and utilization by gram-negative bacterial pathogens. Front Cell Infect Microbiol 9:81. https://doi.org/10.3389/fcimb.2019.00081
Richter K, Schicklberger M, Gescher J (2012) Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl Environ Microbiol 78(4):913–921. https://doi.org/10.1128/AEM.06803-11
Robey M, Cianciotto NP (2002) Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect Immun 70(10):5659–5669
Rocha ER, Bergonia HA, Gerdes S, Jeffrey Smith C (2019) Bacteroides fragilis requires the ferrous-iron transporter FeoAB and the CobN-like proteins BtuS1 and BtuS2 for assimilation of iron released from heme. MicrobiologyOpen 8(4):e00669. https://doi.org/10.1002/mbo3.669
Roden EE, Sobolev D, Glazer B, Luther GW (2004) Potential for microscale bacterial Fe redox cycling at the aerobic-anaerobic interface. Geomicrobiol J 21(6):379–391. https://doi.org/10.1080/01490450490485872
Rong C, Huang Y, Zhang W, Jiang W, Li Y, Li J (2008) Ferrous iron transport protein B gene (feoB1) plays an accessory role in magnetosome formation in Magnetospirillum gryphiswaldense strain MSR-1. Res Microbiol 159(7):530–536. https://doi.org/10.1016/j.resmic.2008.06.005
Rong C, Zhang C, Zhang Y, Qi L, Yang J, Guan G, Li Y, Li J (2012) FeoB2 functions in magnetosome formation and oxidative stress protection in Magnetospirillum gryphiswaldense strain MSR-1. J Bacteriol 194(15):3972–3976. https://doi.org/10.1128/JB.00382-12
Runyen-Janecky LJ, Reeves SA, Gonzales EG, Payne SM (2003) Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect Immun 71(4):1919–1928
Sabri M, Caza M, Proulx J, Lymberopoulos MH, Brée A, Moulin-Schouleur M, Curtiss R 3rd, Dozois CM (2008) Contribution of the SitABCD, MntH, and FeoB metal transporters to the virulence of avian pathogenic Escherichia coli O78 strain chi7122. Infect Immun 76(2):601–611. https://doi.org/10.1128/iai.00789-07
Saier MH, Tran CV, Barabote RD (2006) TCDB: the transporter classification database for membrane transport protein analyses and information. Nucleic Acids Res 34(Database issue):D181–D186. https://doi.org/10.1093/nar/gkj001
Saier MH, Reddy VS, Moreno-Hagelsieb G, Hendargo KJ, Zhang Y, Iddamsetty V, Lam KJK, Tian N, Russum S, Wang J, Medrano-Soto A (2021) The transporter classification database (TCDB): 2021 update. Nucleic Acids Res 49(D1):D461–D467. https://doi.org/10.1093/nar/gkaa1004
Schad M, Konhauser KO, Sánchez-Baracaldo P, Kappler A, Bryce C (2019) How did the evolution of oxygenic photosynthesis influence the temporal and spatial development of the microbial iron cycle on ancient earth? Free Radic Biol Med 140:154–166. https://doi.org/10.1016/j.freeradbiomed.2019.07.014
Schröder I, Johnson E, de Vries S (2003) Microbial ferric iron reductases. FEMS Microbiol Rev 27(2-3):427–447. https://doi.org/10.1016/S0168-6445(03)00043-3
Schüler D, Baeuerlein E (1998) Dynamics of iron uptake and Fe3O4 biomineralization during aerobic and microaerobic growth of Magnetospirillum gryphiswaldense. J Bacteriol 180(1):159–162
Seeliger S, Cord-Ruwisch R, Schink B (1998) A periplasmic and extracellular c-type cytochrome of Geobacter sulfurreducens acts as a ferric iron reductase and as an electron carrier to other acceptors or to partner bacteria. J Bacteriol 180(14):3686–3691. https://doi.org/10.1128/JB.180.14.3686-3691.1998
Sestok AE, Linkous RO, Smith AT (2018) Toward a mechanistic understanding of Feo-mediated ferrous iron uptake. Metallomics 10(7):887–898. https://doi.org/10.1039/c8mt00097b
Sestok AE, Lee MA, Smith AT (2021) Unpublished results
Severance S, Chakraborty S, Kosman DJ (2004) The Ftr1p iron permease in the yeast plasma membrane: orientation, topology and structure-function relationships. Biochem J 380(Pt 2):487–496. https://doi.org/10.1042/BJ20031921
Seyedmohammad S, Born D, Venter H (2014) Expression, purification and functional reconstitution of FeoB, the ferrous iron transporter from Pseudomonas aeruginosa. Protein Expr Purif 101:138–145. https://doi.org/10.1016/j.pep.2014.06.012
Seyedmohammad S, Fuentealba NA, Marriott RA, Goetze TA, Edwardson JM, Barrera NP, Venter H (2016) Structural model of FeoB, the iron transporter from Pseudomonas aeruginosa, predicts a cysteine lined, GTP-gated pore. Biosci Rep 36(2). https://doi.org/10.1042/bsr20160046
Sheldon JR, Heinrichs DE (2015) Recent developments in understanding the iron acquisition strategies of gram positive pathogens. FEMS Microbiol Rev 39(4):592–630. https://doi.org/10.1093/femsre/fuv009
Shih PM (2019) Early cyanobacteria and the innovation of microbial sunscreens. mBio 10(3). https://doi.org/10.1128/mBio.01262-19
Shin M, Mey AR, Payne SM (2019) FeoB contains a dual nucleotide-specific NTPase domain essential for ferrous iron uptake. Proc Natl Acad Sci U S A 116(10):4599–4604. https://doi.org/10.1073/pnas.1817964116
Shin M, Park J, Jin Y, Kim IJ, Payne SM, Kim KH (2020) Biochemical characterization of bacterial FeoBs: a perspective on nucleotide specificity. Arch Biochem Biophys 685:108350. https://doi.org/10.1016/j.abb.2020.108350
Silver S, Kralovic ML (1969) Manganese accumulation by Escherichia coli: evidence for a specific transport system. Biochem Biophys Res Commun 34(5):640–645. https://doi.org/10.1016/0006-291x(69)90786-4
Silver S, Johnseine P, King K (1970) Manganese active transport in Escherichia coli. J Bacteriol 104(3):1299–1306. https://doi.org/10.1128/JB.104.3.1299-1306.1970
Simmons SL, Sievert SM, Frankel RB, Bazylinski DA, Edwards KJ (2004) Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microbiol 70(10):6230–6239. https://doi.org/10.1128/AEM.70.10.6230-6239.2004
Skaar EP (2010) The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6(8):e1000949. https://doi.org/10.1371/journal.ppat.1000949
Smith AT, Sestok AE (2018) Expression and purification of functionally active ferrous iron transporter FeoB from Klebsiella pneumoniae. Protein Expr Purif 142:1–7. https://doi.org/10.1016/j.pep.2017.09.007
Smith RL, Thompson LJ, Maguire ME (1995) Cloning and characterization of MgtE, a putative new class of Mg2+ transporter from Bacillus firmus OF4. J Bacteriol 177(5):1233–1238. https://doi.org/10.1128/jb.177.5.1233-1238.1995
Smith JA, Lovley DR, Tremblay PL (2013) Outer cell surface components essential for Fe(III) oxide reduction by Geobacter metallireducens. Appl Environ Microbiol 79(3):901–907. https://doi.org/10.1128/AEM.02954-12
Smith AT, Linkous RO, Max NJ, Sestok AE, Szalai VA, Chacón KN (2019) The FeoC [4Fe-4S] cluster is redox-active and rapidly oxygen-sensitive. Biochemistry 58(49):4935–4949. https://doi.org/10.1021/acs.biochem.9b00745
Soe CZ, Codd R (2014) Unsaturated macrocyclic dihydroxamic acid siderophores produced by Shewanella putrefaciens using precursor-directed biosynthesis. ACS Chem Biol 9(4):945–956. https://doi.org/10.1021/cb400901j
Spiro S, Guest JR (1990) FNR and its role in oxygen-regulated gene expression in Escherichia coli. FEMS Microbiol Rev 6(4):399–428
Stearman R, Yuan DS, Yamaguchi-Iwai Y, Klausner RD, Dancis A (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271(5255):1552–1557. https://doi.org/10.1126/science.271.5255.1552
Stevenson B, Wyckoff EE, Payne SM (2016) Vibrio cholerae FeoA, FeoB, and FeoC interact to form a complex. J Bacteriol 198(7):1160–1170. https://doi.org/10.1128/jb.00930-15
Sturm A, Schierhorn A, Lindenstrauss U, Lilie H, Brüser T (2006) YcdB from Escherichia coli reveals a novel class of Tat-dependently translocated hemoproteins. J Biol Chem 281(20):13972–13978. https://doi.org/10.1074/jbc.M511891200
Su YC, Chin KH, Hung HC, Shen GH, Wang AH, Chou SH (2010) Structure of Stenotrophomonas maltophilia FeoA complexed with zinc: a unique prokaryotic SH3-domain protein that possibly acts as a bacterial ferrous iron-transport activating factor. Acta Crystallogr Sect F Struct Biol Cryst Commun 66(Pt 6):636–642. https://doi.org/10.1107/s1744309110013941
Suzuki T, Okamura Y, Calugay RJ, Takeyama H, Matsunaga T (2006) Global gene expression analysis of iron-inducible genes in Magnetospirillum magneticum AMB-1. J Bacteriol 188(6):2275–2279. https://doi.org/10.1128/JB.188.6.2275-2279.2006
Suzuki T, Okamura Y, Arakaki A, Takeyama H, Matsunaga T (2007) Cytoplasmic ATPase involved in ferrous ion uptake from magnetotactic bacterium Magnetospirillum magneticum AMB-1. FEBS Lett 581(18):3443–3448. https://doi.org/10.1016/j.febslet.2007.06.047
Taoka A, Umeyama C, Fukumori Y (2009) Identification of iron transporters expressed in the magnetotactic bacterium Magnetospirillum magnetotacticum. Curr Microbiol 58(2):177–181. https://doi.org/10.1007/s00284-008-9305-7
Thomas-Charles CA, Zheng H, Palmer LE, Mena P, Thanassi DG, Furie MB (2013) FeoB-mediated uptake of iron by Francisella tularensis. Infect Immun 81(8):2828–2837. https://doi.org/10.1128/iai.00170-13
Thormann KM, Saville RM, Shukla S, Pelletier DA, Spormann AM (2004) Initial phases of biofilm formation in Shewanella oneidensis MR-1. J Bacteriol 186(23):8096–8104. https://doi.org/10.1128/JB.186.23.8096-8104.2004
Torrents E (2014) Ribonucleotide reductases: essential enzymes for bacterial life. Front Cell Infect Microbiol 4:52. https://doi.org/10.3389/fcimb.2014.00052
Troxell B, Hassan HM (2013) Transcriptional regulation by ferric uptake regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol 3:59. https://doi.org/10.3389/fcimb.2013.00059
Unden G, Achebach S, Holighaus G, Tran HG, Wackwitz B, Zeuner Y (2002) Control of FNR function of Escherichia coli by O2 and reducing conditions. J Mol Microbiol Biotechnol 4(3):263–268
Veeranagouda Y, Husain F, Boente R, Moore J, Smith CJ, Rocha ER, Patrick S, Wexler HM (2014) Deficiency of the ferrous iron transporter FeoAB is linked with metronidazole resistance in Bacteroides fragilis. J Antimicrob Chemother 69(10):2634–2643. https://doi.org/10.1093/jac/dku219
Velayudhan J, Hughes NJ, McColm AA, Bagshaw J, Clayton CL, Andrews SC, Kelly DJ (2000) Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol Microbiol 37(2):274–286
Vetter IR, Wittinghofer A (2001) The guanine nucleotide-binding switch in three dimensions. Science 294(5545):1299–1304. https://doi.org/10.1126/science.1062023
Weaver EA, Wyckoff EE, Mey AR, Morrison R, Payne SM (2013) FeoA and FeoC are essential components of the Vibrio cholerae ferrous iron uptake system, and FeoC interacts with FeoB. J Bacteriol 195(21):4826–4835. https://doi.org/10.1128/jb.00738-13
Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4(10):752–764. https://doi.org/10.1038/nrmicro1490
Wei Y, Fu D (2005) Selective metal binding to a membrane-embedded aspartate in the Escherichia coli metal transporter YiiP (FieF). J Biol Chem 280(40):33716–33724. https://doi.org/10.1074/jbc.M506107200
Winterbourn CC (1995) Toxicity of iron and hydrogen peroxide: the Fenton reaction. Toxicol Lett 82-83:969–974
Wittenberg JB, Bolognesi M, Wittenberg BA, Guertin M (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 277(2):871–874. https://doi.org/10.1074/jbc.R100058200
Xia M, Wei J, Lei Y, Ying L (2007) A novel ferric reductase purified from Magnetospirillum gryphiswaldense MSR-1. Curr Microbiol 55(1):71–75. https://doi.org/10.1007/s00284-007-0023-3
Zhang C, Meng X, Li N, Wang W, Sun Y, Jiang W, Guan G, Li Y (2013) Two bifunctional enzymes with ferric reduction ability play complementary roles during magnetosome synthesis in Magnetospirillum gryphiswaldense MSR-1. J Bacteriol 195(4):876–885. https://doi.org/10.1128/JB.01750-12
Zhou D, Hardt WD, Galán JE (1999) Salmonella typhimurium encodes a putative iron transport system within the centisome 63 pathogenicity island. Infect Immun 67(4):1974–1981
Acknowledgements
This work was supported by NIH R21 DE027803 (A. T. S.), NIH R35 GM133497 (A. T. S.), and in part by NIH T32 GM066706 (A. E. S.).
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Sestok, A.E., Lee, M.A., Smith, A.T. (2022). Prokaryotic Ferrous Iron Transport: Exploiting Pools of Reduced Iron Across Multiple Microbial Environments. 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_12
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