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Heavy Metal Resistance in Prokaryotes: Mechanism and Application

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Microbial Communities and their Interactions in the Extreme Environment

Part of the book series: Microorganisms for Sustainability ((MICRO,volume 32))

Abstract

Metal-rich natural and artificial habitats are extreme environments for the development and evolution of unique microbial communities, which have adapted to the toxic levels of the metals. Diverse bacterial groups have developed abilities to deal with the toxic metals by bioaccumulation of the metal ions inside the cell actively or passively, extracellular precipitation, efflux of heavy metals outside to the microbial cell surface, biotransformation of toxic metals to less toxic forms, and metal adsorption on the cell wall. Metalophilic microbes are found in all bacterial and archaeal groups studied, but mostly appear among aerobic and facultative anaerobic chemoheterotrophic and chemolithoautotrophic microorganisms of the Bacillus, Pseudomonas, Staphylococcus, Actinobacteria, Cuprividus, Acidobacterium, Acidithiobacillus, Thiobacillus, Ferroplasma, and Sulfolobus genera. The phenomenon of microbial heavy metal resistance has fundamental importance and is particularly relevant in microbial ecology, especially in connection with the roles of microbes in biogeochemical cycling of heavy metals and in the bioremediation of metal-contaminated environments. The heavy metal resistance mechanisms and different applications of metal resistant/metalophilic bacteria and archaea have been expounded deeply in this chapter.

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References

  • Adekanmbi AO, Adelowo OO, Okoh AI, Fagade OE (2019) Metal-resistance encoding gene-fingerprints in some bacteria isolated from wastewaters of selected printeries in Ibadan, South-Western Nigeria. J Taibah Univ Sci 13(1):266–273

    Article  Google Scholar 

  • Aguilar-Barajas E, Ramírez-Díaz MI, Riveros-Rosas H, Cervantes C (2010) Heavy metal resistance in pseudomonads. In: Ramos JL, Filloux A (eds) Pseudomonas: volume 6: molecular microbiology, infection and biodiversity. Springer, Dordrecht, pp 255–282

    Google Scholar 

  • Ahemad M (2012) Implications of bacterial resistance against heavy metals in bioremediation: a review. IIOABJ 3(3):39–46

    CAS  Google Scholar 

  • Ahemad M (2015) Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review. 3 Biotech 5(2):111–121

    Article  PubMed  Google Scholar 

  • Akcil A, Erust C, Ozdemiroglu S, Fonti V, Beolchini F (2015) A review of approaches and techniques used in aquatic contaminated sediments: metal removal and stabilization by chemical and biotechnological processes. J Clean Prod 86:24–36

    Article  CAS  Google Scholar 

  • Ali H, Khan E (2018) What are heavy metals? Long-standing controversy over the scientific use of the term ‘heavy metals’—proposal of a comprehensive definition. Toxicol Environ Chem 100(1):6–19

    Article  CAS  Google Scholar 

  • Anderson GL, Love M, Zeider BK (2003) Metabolic energy from arsenite oxidation in Alcaligenes faecalis. J Phys IV (Proc) 107:49–52

    CAS  Google Scholar 

  • Anton A, Grosse C, Reissmann J, Pribyl T, Nies DH (1999) CzcD is a heavy metal ion transporter involved in regulation of heavy metal resistance in Ralstonia sp. strain CH34. J Bacteriol 181(22):6876–6881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Argüello JM, Mandal AK, Mana-Capelli S (2003) Heavy metal transport CPx-ATPases from the thermophile Archaeoglobus fulgidus. Ann N Y Acad Sci 986:212–218

    Article  PubMed  Google Scholar 

  • Argüello JM, Raimunda D, Padilla-Benavides T (2013) Mechanisms of copper homeostasis in bacteria. Front Cell Infect Microbiol 3:73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baldwin DR, Marshall WJ (1999) Heavy metal poisoning and its laboratory investigation. Ann Clin Biochem 36(Pt 3):267–300

    Article  CAS  PubMed  Google Scholar 

  • Bartolucci S, Contursi P, Fiorentino G, Limauro D, Pedone E (2013) Responding to toxic compounds: a genomic and functional overview of archaea. Front Biosci (Landmark Ed) 18:165–189

    Article  CAS  Google Scholar 

  • Ben Fekih I, Zhang C, Li YP, Zhao Y, Alwathnani HA, Saquib Q, Rensing C, Cervantes C (2018) Distribution of arsenic resistance genes in prokaryotes. Front Microbiol 9:2473

    Article  PubMed  PubMed Central  Google Scholar 

  • Bini E (2010) Archaeal transformation of metals in the environment. FEMS Microbiol Ecol 73(1):1–16

    CAS  PubMed  Google Scholar 

  • Boyd ES, Barkay T (2012) The mercury resistance operon: from an origin in a geothermal environment to an efficient detoxification machine. Front Microbiol 3:349

    Article  PubMed  PubMed Central  Google Scholar 

  • Branco R, Chung A-P, Morais PV (2008) Sequencing and expression of two arsenic resistance operons with different functions in the highly arsenic-resistant strain Ochrobactrum tritici SCII24T. BMC Microbiol 8(1):95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brown NL, Stoyanov JV, Kidd SP, Hobman JL (2003) The MerR family of transcriptional regulators. FEMS Microbiol Rev 27(2–3):145–163

    Article  CAS  PubMed  Google Scholar 

  • Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45(3):198–207

    Article  CAS  PubMed  Google Scholar 

  • Butcher BG, Rawlings DE (2002) The divergent chromosomal ars operon of Acidithiobacillus ferrooxidans is regulated by an atypical ArsR protein. Microbiology (Reading) 148(Pt 12):3983–3992

    Article  CAS  Google Scholar 

  • Butcher BG, Deane SM, Rawlings DE (2000) The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol 66(5):1826–1833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai J, Salmon K, DuBow MS (1998) A chromosomal ars operon homologue of Pseudomonas aeruginosa confers increased resistance to arsenic and antimony in Escherichia coli. Microbiology (Reading) 144(Pt 10):2705–2713

    Article  CAS  Google Scholar 

  • Carlin A, Shi W, Dey S, Rosen BP (1995) The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177(4):981–986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cazorla FM, Romero D, Pérez-García A, Lugtenberg BJJ, Vicente A d, Bloemberg G (2007) Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J Appl Microbiol 103(5):1950–1959

    Article  CAS  PubMed  Google Scholar 

  • Cervantes C, Campos-García J (2007) Reduction and efflux of chromate by bacteria. In: Nies DH, Silver S (eds) Molecular microbiology of heavy metals. Springer, Berlin, pp 407–419

    Chapter  Google Scholar 

  • Chen CM, Misra TK, Silver S, Rosen BP (1986) Nucleotide sequence of the structural genes for an anion pump. The plasmid-encoded arsenical resistance operon. J Biol Chem 261(32):15030–15038

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Ren Y, Lin J, Liu X, Pang X (2012) Acidithiobacillus caldus sulfur oxidation model based on transcriptome analysis between the wild type and sulfur oxygenase reductase defective mutant. PLoS One 7(9):e39470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chmurny AB, Quintero EJ, Kneer R (1998) Novel heavy metals sorbents produced from hyphomonas and method of use. Worldwide applications

    Google Scholar 

  • Collard JM, Corbisier P, Diels L, Dong Q, Jeanthon C, Mergeay M, Taghavi S, van der Lelie D, Wilmotte A, Wuertz S (1994) Plasmids for heavy metal resistance in Alcaligenes eutrophus CH34: mechanisms and applications. FEMS Microbiol Rev 14(4):405–414

    Article  CAS  PubMed  Google Scholar 

  • Cooksey DA (1994) Molecular mechanisms of copper resistance and accumulation in bacteria. FEMS Microbiol Rev 14(4):381–386

    Article  CAS  PubMed  Google Scholar 

  • Coombs JM, Barkay T (2005) New findings on evolution of metal homeostasis genes: evidence from comparative genome analysis of Bacteria and archaea. Appl Environ Microbiol 71(11):7083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cousins RJ, Liuzzi JP, Lichten LA (2006) Mammalian zinc transport, trafficking, and signals. J Biol Chem 281(34):24085–24089

    Article  CAS  PubMed  Google Scholar 

  • Cuebas M, Villafane A, McBride M, Yee N, Bini E (2011) Arsenate reduction and expression of multiple chromosomal ars operons in Geobacillus kaustophilus A1. Microbiology (Reading) 157(Pt 7):2004–2011

    Article  CAS  Google Scholar 

  • De Hertogh B, Lantin A-C, Baret PV, Goffeau A (2004) The archaeal P-type ATPases. J Bioenerg Biomembr 36(1):135–142

    Article  PubMed  Google Scholar 

  • De Philippis R, Paperi R, Sili C (2007) Heavy metal sorption by released polysaccharides and whole cultures of two exopolysaccharide-producing cyanobacteria. Biodegradation 18(2):181–187

    Article  CAS  PubMed  Google Scholar 

  • Dhawan IK, Roy R, Koehler BP, Mukund S, Adams MW, Johnson MK (2000) Spectroscopic studies of the tungsten-containing formaldehyde ferredoxin oxidoreductase from the hyperthermophilic archaeon Thermococcus litoralis. J Biol Inorg Chem 5(3):313–327

    Article  CAS  PubMed  Google Scholar 

  • Díaz-Magaña A, Aguilar-Barajas E, Moreno-Sánchez R, Ramírez-Díaz MI, Riveros-Rosas H, Vargas E, Cervantes C (2009) Short-chain chromate ion transporter proteins from Bacillus subtilis confer chromate resistance in Escherichia coli. J Bacteriol 191(17):5441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Díaz-Pérez C, Cervantes C, Campos-García J, Julián-Sánchez A, Riveros-Rosas H (2007) Phylogenetic analysis of the chromate ion transporter (CHR) superfamily. FEBS J 274(23):6215–6227

    Article  PubMed  CAS  Google Scholar 

  • Diekert G, Konheiser U, Piechulla K, Thauer RK (1981) Nickel requirement and factor F430 content of methanogenic bacteria. J Bacteriol 148(2):459–464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diels L, Dong Q, van der Lelie D, Baeyens W, Mergeay M (1995) Theczc operon of Alcaligenes eutrophus CH34: from resistance mechanism to the removal of heavy metals. J Ind Microbiol 14(2):142–153

    Article  CAS  PubMed  Google Scholar 

  • Drewniak L, Dziewit L, Ciezkowska M, Gawor J, Gromadka R, Sklodowska A (2013) Structural and functional genomics of plasmid pSinA of Sinorhizobium sp. M14 encoding genes for the arsenite oxidation and arsenic resistance. J Biotechnol 164(4):479–488

    Article  CAS  PubMed  Google Scholar 

  • Ehrlich HL (1997a) Microbes and metals. Appl Microbiol Biotechnol 48(6):687–692

    Article  CAS  Google Scholar 

  • Ehrlich HL (1997b) Technical potential for bioleaching and biobeneficiation of ores to recover base metals (other than iron or copper), platinum-group metals and silver. In: Rawlings DE (ed) Biomining: theory, microbes and industrial processes. Springer, Berlin, pp 129–150

    Chapter  Google Scholar 

  • Eitinger T, Mandrand-Berthelot MA (2000) Nickel transport systems in microorganisms. Arch Microbiol 173(1):1–9

    Article  CAS  PubMed  Google Scholar 

  • 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(12):3707–3710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feinberg LF, Srikanth R, Vachet RW, Holden JF (2008) Constraints on anaerobic respiration in the hyperthermophilic archaea Pyrobaculum islandicum and Pyrobaculum aerophilum. Appl Environ Microbiol 74(2):396–402

    Article  CAS  PubMed  Google Scholar 

  • Freedman Z, Zhu C, Barkay T (2012) Mercury resistance and mercuric reductase activities and expression among chemotrophic thermophilic Aquificae. Appl Environ Microbiol 78(18):6568–6575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freire-Nordi CS, Vieira AAH, Nascimento OR (2005) The metal binding capacity of Anabaena spiroides extracellular polysaccharide: an EPR study. Process Biochem 40(6):2215–2224

    Article  CAS  Google Scholar 

  • Gadd G (2005) Microorganisms in toxic metal-polluted soils. In: Varma A, Buscot F (eds) Microorganisms in soils: roles in genesis and functions soil biology. Springer, Berlin, pp 325–356

    Chapter  Google Scholar 

  • Garbinski LD, Rosen BP, Chen J (2019) Pathways of arsenic uptake and efflux. Environ Int 126:585–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gavrilescu M (2004) Removal of heavy metals from the environment by biosorption. Eng Life Sci 4(3):219–232

    Article  CAS  Google Scholar 

  • Gihring TM, Bond PL, Peters SC, Banfield JF (2003) Arsenic resistance in the archaeon “Ferroplasma acidarmanus”: new insights into the structure and evolution of the ars genes. Extremophiles 7(2):123–130

    Article  CAS  PubMed  Google Scholar 

  • Golyshina OV, Pivovarova TA, Karavaiko GI, Kondratéva TF, Moore ER, Abraham WR, Lünsdorf H, Timmis KN, Yakimov MM, Golyshin PN (2000) Ferroplasma acidiphilum gen. Nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. Nov., comprising a distinct lineage of the archaea. Int J Syst Evol Microbiol 50(Pt 3):997–1006

    Article  CAS  PubMed  Google Scholar 

  • Grass G, Fan B, Rosen BP, Franke S, Nies DH, Rensing C (2001) ZitB (YbgR), a member of the cation diffusion facilitator family, is an additional zinc transporter in Escherichia coli. J Bacteriol 183(15):4664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guffanti AA, Wei Y, Rood SV, Krulwich TA (2002) An antiport mechanism for a member of the cation diffusion facilitator family: divalent cations efflux in exchange for K+ and H+. Mol Microbiol 45(1):145–153

    Article  CAS  PubMed  Google Scholar 

  • Gupta P, Diwan B (2017) Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep (Amst) 13:58–71

    Article  Google Scholar 

  • Gutierrez T, Biller DV, Shimmield T, Green DH (2012) Metal binding properties of the EPS produced by Halomonas sp. TG39 and its potential in enhancing trace element bioavailability to eukaryotic phytoplankton. Biometals 25(6):1185–1194

    Article  CAS  PubMed  Google Scholar 

  • Ha J, Gélabert A, Spormann AM, Brown GE (2010) Role of extracellular polymeric substances in metal ion complexation on Shewanella oneidensis: batch uptake, thermodynamic modeling, ATR-FTIR, and EXAFS study. Geochim Cosmochim Acta 74(1):1–15

    Article  CAS  Google Scholar 

  • Hantke K (2001) Bacterial zinc transporters and regulators. Biometals 14(3):239–249

    Article  CAS  PubMed  Google Scholar 

  • Hartzell PL, Escalante-Semerena JC, Bobik TA, Wolfe RS (1988) A simplified methylcoenzyme M methylreductase assay with artificial electron donors and different preparations of component C from Methanobacterium thermoautotrophicum delta H. J Bacteriol 170(6):2711–2715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkes SJ (1997) What is a “heavy metal”? J Chem Educ 74(11):1374

    Article  CAS  Google Scholar 

  • Hedges RW, Baumberg S (1973) Resistance to arsenic compounds conferred by a plasmid transmissible between strains of Escherichia coli. J Bacteriol 115(1):459–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hohle TH, O'Brian MR (2009) The mntH gene encodes the major Mn(2+) transporter in Bradyrhizobium japonicum and is regulated by manganese via the Fur protein. Mol Microbiol 72(2):399–409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hrynkiewicz K, Złoch M, Kowalkowski T, Baum C, Niedojadło K, Buszewski B (2015) Strain-specific bioaccumulation and intracellular distribution of Cd2+ in bacteria isolated from the rhizosphere, ectomycorrhizae, and fruitbodies of ectomycorrhizal fungi. Environ Sci Pollut Res Int 22(4):3055–3067

    Article  CAS  PubMed  Google Scholar 

  • Huber G, Stetter KO (1991) Sulfolobus metallicus, sp. nov., a novel strictly chemolithoautotrophic thermophilic archaeal species of metal-mobilizers. Syst Appl Microbiol 14(4):372–378

    Article  CAS  Google Scholar 

  • Huber G, Spinnler C, Gambacorta A, Stetter KO (1989) Metallosphaera sedula gen, and sp. nov. represents a new genus of aerobic, metal-mobilizing, thermoacidophilic archaebacteria. Syst Appl Microbiol 12(1):38–47

    Article  Google Scholar 

  • Hynninen A (2010) Zinc, cadmium and lead resistance mechanisms in bacteria and their contribution to biosensing. Academic Dissertation in Microbiology, University of Helsinki. pp 1–52

    Google Scholar 

  • Ianeva OD (2009) Mechanisms of bacteria resistance to heavy metals. Mikrobiol Zh 71(6):54–65

    CAS  Google Scholar 

  • Igiri BE, Okoduwa SIR, Idoko GO, Akabuogu EP, Adeyi AO, Ejiogu IK (2018) Toxicity and bioremediation of heavy metals contaminated ecosystem from tannery wastewater: a review. Hindawi J Toxicol 2018:2568038

    Google Scholar 

  • Incharoensakdi A, Kitjaharn P (2002) Zinc biosorption from aqueous solution by a halotolerant cyanobacterium Aphanothece halophytica. Curr Microbiol 45(4):261–264

    Article  CAS  PubMed  Google Scholar 

  • Ji G, Silver S (1992) Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258. J Bacteriol 174(11):3684–3694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kachur AV, Koch CJ, Biaglow JE (1998) Mechanism of copper-catalyzed oxidation of glutathione. Free Radic Res 28(3):259–269

    Article  CAS  PubMed  Google Scholar 

  • Karnachuk OV, Kurochkina SY, Nicomrat D, Frank YA, Ivasenko DA, Phyllipenko EA, Tuovinen OH (2003) Copper resistance in Desulfovibrio strain R2. Antonie Van Leeuwenhoek 83(1):99–106

    Article  CAS  PubMed  Google Scholar 

  • Kashefi K, Moskowitz BM, Lovley DR (2008) Characterization of extracellular minerals produced during dissimilatory Fe(III) and U(VI) reduction at 100 °C by Pyrobaculum islandicum. Geobiology 6(2):147–154

    Article  CAS  PubMed  Google Scholar 

  • Kasprzak KS (2002) Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis1, 3 1 This article is part of a series of reviews on “Oxidative DNA Damage and Repair.” The full list of papers may be found on the homepage of the journal. 3Guest Editor: Miral Dizdaroglu. Free Radic Biol Med 32(10):958–967

    Article  CAS  PubMed  Google Scholar 

  • Kaur A, Pan M, Meislin M, Facciotti MT, El-Gewely R, Baliga NS (2006) A systems view of haloarchaeal strategies to withstand stress from transition metals. Genome Res 16(7):841–854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Oves M (2012) Erratum to: role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 10(1):105–106

    Article  CAS  Google Scholar 

  • Kim S-Y, Kim J-H, Kim C-J, Oh D-K (1996) Metal adsorption of the polysaccharide produced from Methylobacterium organophilum. Biotechnol Lett 18(10):1161–1164

    Article  CAS  Google Scholar 

  • Kletzin A, Adams MW (1996) Tungsten in biological systems. FEMS Microbiol Rev 18(1):5–63

    Article  CAS  PubMed  Google Scholar 

  • Krom BP, Warner JB, Konings WN, Lolkema JS (2000) Complementary metal ion specificity of the metal-citrate transporters CitM and CitH of Bacillus subtilis. J Bacteriol 182(22):6374–6381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lau CK, Krewulak KD, Vogel HJ (2016) Bacterial ferrous iron transport: the Feo system. FEMS Microbiol Rev 40(2):273–298

    Article  CAS  PubMed  Google Scholar 

  • Le TT, Son M-H, Nam I-H, Yoon H, Kang Y-G, Chang Y-S (2017) Transformation of hexabromocyclododecane in contaminated soil in association with microbial diversity. J Hazard Mater 325:82–89

    Article  CAS  PubMed  Google Scholar 

  • Lee SW, Glickmann E, Cooksey DA (2001) Chromosomal locus for cadmium resistance in Pseudomonas putida consisting of a cadmium-transporting ATPase and a MerR family response regulator. Appl Environ Microbiol 67(4):1437–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Krumholz LR (2007) Regulation of arsenate resistance in Desulfovibrio desulfuricans G20 by an arsRBCC operon and an arsC gene. J Bacteriol 189(10):3705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo J-H, Wu M, Liu J, Qian G, Yuan Z, Guo J (2019) Microbial chromate reduction coupled with anaerobic oxidation of methane in a membrane biofilm reactor. Environ Int 130:104926

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manage 174:14–25

    Article  CAS  PubMed  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69(2):220–228

    Article  CAS  PubMed  Google Scholar 

  • Mana-Capelli S, Mandal AK, Argüello JM (2003) Archaeoglobus fulgidus CopB is a thermophilic Cu2+-ATPase: functional role of its histidine-rich-N-terminal metal binding domain. J Biol Chem 278(42):40534–40541

    Article  CAS  PubMed  Google Scholar 

  • Mandal AK, Argüello JM (2003) Functional roles of metal binding domains of the Archaeoglobus fulgidus cu(+)-ATPase CopA. Biochemistry 42(37):11040–11047

    Article  CAS  PubMed  Google Scholar 

  • Marchal M, Briandet R, Koechler S, Kammerer B, Bertin PN (2010) Effect of arsenite on swimming motility delays surface colonization in Herminiimonas arsenicoxydans. Microbiology 156(8):2336–2342

    Article  CAS  PubMed  Google Scholar 

  • Margaryan AA, Panosyan HH, Birkeland N-K, Trchounian AH (2013) Heavy metal accumulation and the expression of the copA and nikA genes in Bacillus subtilis AG4 isolated from the Sotk gold min in Armenia. Yerevan, Armenia: biolog. J Armenia 3(65):51–57

    Google Scholar 

  • Meija J, Coplen TB, Berglund M, Brand WA, De Bièvre P, Gröning M, Holden NE, Irrgeher J, Loss RD, Walczyk T, Prohaska T (2016) Atomic weights of the elements 2013 (IUPAC technical report). Pure Appl Chem 88(3):265–291

    Article  CAS  Google Scholar 

  • Mills SD, Lim C-K, Cooksey DA (1994) Purification and characterization of CopR, a transcriptional activator protein that binds to a conserved domain (cop box) in copper- inducible promoters of Pseudomonas syringae. Mol Gen Genet 244(4):341–351

    Article  CAS  PubMed  Google Scholar 

  • Moffett JW, Brand LE (1996) Production of strong, extracellular cu chelators by marine cyanobacteria in response to cu stress. Limnol Oceanogr 41(3):388–395

    Article  CAS  Google Scholar 

  • Moraleda-Muñoz A, Pérez J, Extremera AL, Muñoz-Dorado J (2010) Differential regulation of six heavy metal efflux Systems in the Response of Myxococcus xanthus to copper. Appl Environ Microbiol 76(18):6069

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mourão J, Rebelo A, Ribeiro S, Peixe L, Novais C, Antunes P (2020) Tolerance to arsenic contaminant among multidrug-resistant and copper-tolerant salmonella successful clones is associated with diverse ars operons and genetic contexts. Environ Microbiol 22(7):2829–2842

    Article  PubMed  CAS  Google Scholar 

  • Muller D, Médigue C, Koechler S, Barbe V, Barakat M, Talla E, Bonnefoy V, Krin E, Arsène-Ploetze F, Carapito C, Chandler M, Cournoyer B, Cruveiller S, Dossat C, Duval S, Heymann M, Leize E, Lieutaud A, Lièvremont D, Makita Y, Mangenot S, Nitschke W, Ortet P, Perdrial N, Schoepp B, Siguier P, Simeonova DD, Rouy Z, Segurens B, Turlin E, Vallenet D, Van Dorsselaer A, Weiss S, Weissenbach J, Lett MC, Danchin A, Bertin PN (2007) A tale of two oxidation states: bacterial colonization of arsenic-rich environments. PLoS Genet 3(4):e53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27(2–3):239–261

    Article  CAS  PubMed  Google Scholar 

  • Nadar VS, Yoshinaga M, Pawitwar SS, Kandavelu P, Sankaran B, Rosen BP (2016) Structure of the ArsI C-as Lyase: insights into the mechanism of degradation of Organoarsenical herbicides and growth promoters. J Mol Biol 428(11):2462–2473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naik S, Furtado I (2014) Equilibrium and kinetics of adsorption of Mn2+ by Haloarchaeon Halobacterium sp. GUSF (MTCC3265). Geomicrobiol J 31(8):708–715

    Article  CAS  Google Scholar 

  • Naik MM, Pandey A, Dubey SK (2012) Pseudomonas aeruginosa strain WI-1 from Mandovi estuary possesses metallothionein to alleviate lead toxicity and promotes plant growth. Ecotoxicol Environ Saf 79:129–133

    Article  CAS  PubMed  Google Scholar 

  • Ndeddy Aka RJ, Babalola OO (2016) Effect of bacterial inoculation of strains of Pseudomonas aeruginosa, Alcaligenes feacalis and Bacillus subtilis on germination, growth and heavy metal (cd, cr, and ni) uptake of brassica juncea. Int J Phytoremediation 18(2):200–209

    Article  CAS  PubMed  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51(6):730–750

    Article  CAS  PubMed  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27(2–3):313–339

    Article  CAS  PubMed  Google Scholar 

  • Nies D (2007) Bacterial transition metal homeostasis. In: Nies D, Silver S (eds) Molecular microbiology of heavy metals microbiology monographs. Springer, Berlin, pp 117–142

    Chapter  Google Scholar 

  • Nies DH, Silver S (1995) Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol 14(2):186–199

    Article  CAS  PubMed  Google Scholar 

  • Nikaido H (2018) RND transporters in the living world. Res Microbiol 169(7–8):363–371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norris PR, Clark DA, Owen JP, Waterhouse S (1996) Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiology (Reading) 142(Pt 4):775–783

    Article  CAS  Google Scholar 

  • Novick RP, Roth C (1968) Plasmid-linked resistance to inorganic salts in Staphylococcus aureus. J Bacteriol 95(4):1335–1342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okoduwa SIR, Igiri B, Udeh CB, Edenta C, Gauje B (2017) Tannery effluent treatment by yeast species isolates from watermelon. Toxics 5(1)

    Google Scholar 

  • Ordóñez E, Letek M, Valbuena N, Gil JA, Mateos LM (2005) Analysis of genes involved in arsenic resistance in Corynebacterium glutamicum ATCC 13032. Appl Environ Microbiol 71(10):6206–6215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oremland RS, Stolz JF (2005) Arsenic, microbes and contaminated aquifers. Trends Microbiol 13(2):45–49

    Article  CAS  PubMed  Google Scholar 

  • Oshima T, Kondo K, Ohto K, Inoue K, Baba Y (2008) Preparation of phosphorylated bacterial cellulose as an adsorbent for metal ions. React Funct Polym 68(1):376–383

    Article  CAS  Google Scholar 

  • Ozdemir G, Ozturk T, Ceyhan N, Isler R, Cosar T (2003) Heavy metal biosorption by biomass of Ochrobactrum anthropi producing exopolysaccharide in activated sludge. Bioresour Technol 90(1):71–74

    Article  CAS  PubMed  Google Scholar 

  • Páez-Espino AD, Durante-Rodríguez G, de Lorenzo V (2015) Functional coexistence of twin arsenic resistance systems in Pseudomonas putida KT2440. Environ Microbiol 17(1):229–238

    Article  PubMed  CAS  Google Scholar 

  • Paulsen IT, Saier MH Jr (1997) A novel family of ubiquitous heavy metal ion transport proteins. J Membr Biol 156(2):99–103

    Article  CAS  PubMed  Google Scholar 

  • Peng ED, Oram DM, Battistel MD, Lyman LR, Freedberg DI, Schmitt MP (2018) Iron and zinc regulate expression of a putative ABC metal transporter in Corynebacterium diphtheriae. J Bacteriol 200(10):e00051–e00018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porcheron G, Garenaux A, Proulx J, Sabri M, Dozois C (2013) Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence. Front Cell Infect Microbiol 3:90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pourret O, Hursthouse A (2019) It’s time to replace the term “heavy metals” with “potentially toxic elements” when reporting environmental research. Int J Environ Res Public Health 16(22):4446

    Article  CAS  PubMed Central  Google Scholar 

  • Pradhan SK, Singh NR, Rath BP, Thatoi H (2016) Bacterial chromate reduction: a review of important genomic, proteomic, and bioinformatic analysis. Crit Rev Environ Sci Technol 46(21–22):1659–1703

    Article  CAS  Google Scholar 

  • Prithivirajsingh S, Mishra SK, Mahadevan A (2001) Detection and analysis of chromosomal arsenic resistance in Pseudomonas fluorescens strain MSP3. Biochem Biophys Res Commun 280(5):1393–1401

    Article  CAS  PubMed  Google Scholar 

  • Qin J, Rosen BP, Zhang Y, Wang G, Franke S, Rensing C (2006) Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci U S A 103(7):2075–2080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quatrini R, Johnson DB (2019) Acidithiobacillus ferrooxidans. Trends Microbiol 27(3):282–283

    Article  CAS  PubMed  Google Scholar 

  • Rademacher C, Masepohl B (2012) Copper-responsive gene regulation in bacteria. Microbiology 158:2451–2464

    Article  CAS  PubMed  Google Scholar 

  • Rasulov BA, Yili A, Aisa HA (2013) Biosorption of metal ions by exopolysaccharide produced by Azotobacter chroococcum XU1. J Environ Prot 4:989–993

    Article  CAS  Google Scholar 

  • Raungsomboon S, Chidthaisong A, Bunnag B, Inthorn D, Harvey NW (2006) Production, composition and Pb2+ adsorption characteristics of capsular polysaccharides extracted from a cyanobacterium Gloeocapsa gelatinosa. Water Res 40(20):3759–3766

    Article  CAS  PubMed  Google Scholar 

  • Rosen BP (2002) Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comp Biochem Physiol A Mol Integr Physiol 133(3):689–693

    Article  PubMed  Google Scholar 

  • Rosenstein R, Peschel A, Wieland B, Götz F (1992) Expression and regulation of the antimonite, arsenite, and arsenate resistance operon of Staphylococcus xylosus plasmid pSX267. J Bacteriol 174(11):3676–3683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouch DA, Lee BTO, Morby AP (1995) Understanding cellular responses to toxic agents: a model for mechanism-choice in bacterial metal resistance. J Ind Microbiol 14(2):132–141

    Article  CAS  PubMed  Google Scholar 

  • Ruangsomboon S, Chidthaisong A, Bunnag B, Inthorn D, Harvey NW (2007) Lead (Pb2+) adsorption characteristics and sugar composition of capsular polysaccharides of cyanobacterium Calothrix marchica. Songklanakarin J Sci Technol 29(2):529–541

    Google Scholar 

  • Ryan D, Colleran E (2002) Arsenical resistance in the IncHI2 plasmids. Plasmid 47(3):234–240

    Article  CAS  PubMed  Google Scholar 

  • Salehizadeh H, Shojaosadati SA (2003) Removal of metal ions from aqueous solution by polysaccharide produced from Bacillus firmus. Water Res 37(17):4231–4235

    Article  CAS  PubMed  Google Scholar 

  • Saltikov CW, Cifuentes A, Venkateswaran K, Newman DK (2003) The ars detoxification system is advantageous but not required for as(V) respiration by the genetically tractable Shewanella species strain ANA-3. Appl Environ Microbiol 69(5):2800–2809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samuelson P, Wernérus H, Svedberg M, Ståhl S (2000) Staphylococcal surface display of metal-binding polyhistidyl peptides. Appl Environ Microbiol 66(3):1243–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sand W, Rohde K, Sobotke B, Zenneck C (1992) Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 58(1):85–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sar P, Kazy SK, Asthana RK, Singh SP (1998) Nickel uptake by Pseudomonas aeruginosa: role of modifying factors. Curr Microbiol 37(5):306–311

    Article  CAS  PubMed  Google Scholar 

  • Saravanakumar D, Vijayakumar C, Kumar N, Samiyappan R (2007) PGPR-induced defense responses in the tea plant against blister blight disease. Crop Prot 26(4):556–565

    Article  Google Scholar 

  • Sato T, Kobayashi Y (1998) The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J Bacteriol 180(7):1655–1661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schenk PM, Carvalhais LC, Kazan K (2012) Unraveling plant–microbe interactions: can multi-species transcriptomics help? Trends Biotechnol 30(3):177–184

    Article  CAS  PubMed  Google Scholar 

  • Scherer J, Nies DH (2009) CzcP is a novel efflux system contributing to transition metal resistance in Cupriavidus metallidurans CH34. Mol Microbiol 73(4):601–621

    Article  CAS  PubMed  Google Scholar 

  • Segerer A, Neuner A, Kristjansson JK, Stetter KO (1986) Acidianus infernus gen. Nov., sp. nov., and Acidianus brierleyi comb. nov.: facultatively aerobic, extremely acidophilic thermophilic sulfur-metabolizing archaebacteria. Int J Syst Evol Microbiol 36(4):559–564

    Google Scholar 

  • Sharma M, Kaushik A, Somvir B, K. and Kamra, A. (2008) Sequestration of chromium by exopolysaccharides of Nostoc and Gloeocapsa from dilute aqueous solutions. J Hazard Mater 157(2):315–318

    Article  CAS  PubMed  Google Scholar 

  • Sher S, Rehman A (2019) Use of heavy metals resistant bacteria-a strategy for arsenic bioremediation. Appl Microbiol Biotechnol 103(15):6007–6021

    Article  CAS  PubMed  Google Scholar 

  • Silver S (1996) Bacterial resistances to toxic metal ions. Gene 179(1):9–19

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Dong H, Liu D, Zhao L, Marts AR, Farquhar E, Tierney DL, Almquist CB, Briggs BR (2015) Reduction of hexavalent chromium by the thermophilic methanogen Methanothermobacter thermautotrophicus. Geochim Cosmochim Acta 148:442–456

    Article  CAS  PubMed  Google Scholar 

  • Smith RL, Maguire ME (1995) Distribution of the CorA Mg2+ transport system in gram-negative bacteria. J Bacteriol 177(6):1638–1640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spada S, Pembroke JT, Wall JG (2002) Isolation of a novel Thermus thermophilus metal efflux protein that improves Escherichia coli growth under stress conditions. Extremophiles 6(4):301–308

    Article  CAS  PubMed  Google Scholar 

  • Suzuki K, Wakao N, Kimura T, Sakka K, Ohmiya K (1998) Expression and regulation of the arsenic resistance operon of Acidiphilium multivorum AIU 301 plasmid pKW301 in Escherichia coli. Appl Environ Microbiol 64(2):411–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tavares MT, Neves IC (2008) Biosorption system produced from biofilms supported on Faujasite (FAU) zeolite, process for obtaining it and its usage for removal of hexavalent chromium (Cr(VI)). International patent, W0 2007/020588 A1, EP1912905

    Google Scholar 

  • Tsai KJ, Yoon KP, Lynn AR (1992) ATP-dependent cadmium transport by the cadA cadmium resistance determinant in everted membrane vesicles of Bacillus subtilis. J Bacteriol 174(1):116–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuffin IM, de Groot P, Deane SM, Rawlings DE (2005) An unusual Tn21-like transposon containing an ars operon is present in highly arsenic-resistant strains of the biomining bacterium Acidithiobacillus caldus. Microbiology (Reading) 151(Pt 9):3027–3039

    Article  CAS  Google Scholar 

  • Tuffin IM, Hector SB, Deane SM, Rawlings DE (2006) Resistance determinants of a highly arsenic-resistant strain of Leptospirillum ferriphilum isolated from a commercial biooxidation tank. Appl Environ Microbiol 72(3):2247–2253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turpeinen R, Kairesalo T, Häggblom MM (2004) Microbial community structure and activity in arsenic-, chromium- and copper-contaminated soils. FEMS Microbiol Ecol 47(1):39–50

    Article  CAS  PubMed  Google Scholar 

  • Vardanyan NS, Vardanyan AK (2018) Thermophilic chemolithotrophic bacteria in mining sites. In: Egamberdieva D, Birkeland N-K, Panosyan H, Li W-J (eds) Extremophiles in Eurasian ecosystems: ecology, diversity, and applications. Springer, Singapore, pp 187–218

    Google Scholar 

  • Vargas M, Kashefi K, Blunt-Harris EL, Lovley DR (1998) Microbiological evidence for Fe(III) reduction on early earth. Nature 395(6697):65–67

    Article  CAS  PubMed  Google Scholar 

  • Voica DM, Bartha L, Banciu HL, Oren A (2016) Heavy metal resistance in halophilic Bacteria and archaea. FEMS Microbiol Lett 363(14):1–9

    Article  CAS  Google Scholar 

  • Volesky B (1994) Advances in biosorption of metals: selection of biomass types. FEMS Microbiol Rev 14(4):291–302

    Article  CAS  PubMed  Google Scholar 

  • von Rozycki T, Nies DH (2009) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek 96(2):115–139

    Article  CAS  Google Scholar 

  • Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27(2):195–226

    Article  PubMed  CAS  Google Scholar 

  • Wang G, Kennedy SP, Fasiludeen S, Rensing C, DasSarma S (2004) Arsenic resistance in Halobacterium sp. strain NRC-1 examined by using an improved gene knockout system. J Bacteriol 186(10):3187–3194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Chen S, Xiao X, Huang X, You D, Zhou X, Deng Z (2006) arsRBOCT arsenic resistance system encoded by linear plasmid pHZ227 in Streptomyces sp. strain FR-008. Appl Environ Microbiol 72(5):3738–3742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wani PA, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol 48(11):3262–3267

    Article  CAS  PubMed  Google Scholar 

  • Whelan KF, Colleran E (1992) Restriction endonuclease mapping of the HI2 incompatibility group plasmid R478. J Bacteriol 174(4):1197–1204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White C, Gadd GM (2000) Copper accumulation by sulfate-reducing bacterial biofilms. FEMS Microbiol Lett 183(2):313–318

    Article  CAS  PubMed  Google Scholar 

  • Xiong A, Jayaswal RK (1998) Molecular characterization of a chromosomal determinant conferring resistance to zinc and cobalt ions in Staphylococcus aureus. J Bacteriol 180(16):4024–4029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang HC, Rosen BP (2016) New mechanisms of bacterial arsenic resistance. Biom J 39(1):5–13

    Google Scholar 

  • Yang HC, Cheng J, Finan TM, Rosen BP, Bhattacharjee H (2005) Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J Bacteriol 187(20):6991–6997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Zhao D, Yang J, Wang W, Chen P, Zhang S, Yan L (2019) Acidithiobacillus thiooxidans and its potential application. Appl Microbiol Biotechnol 103(19):7819–7833

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Yang H-C, Rosen BP, Bhattacharjee H (2007) Crystal structure of the flavoprotein ArsH from Sinorhizobium meliloti. FEBS Lett 581(21):3996–4000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng W, Zhang S, Xia M, Wu X, Qiu G, Shen L (2020) Insights into the production of extracellular polymeric substances of Cupriavidus pauculus 1490 under the stimulation of heavy metal ions. RSC Adv 10(34):20385–20394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN (2009) Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genomics 10(1):78

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the Eurasia Programme of the Norwegian Center for International Cooperation in Education (CPEA-2011/10081, CPEA-LT-2016/10095) and partially supported by Research Grant from MESCS Science Committee of Armenia, to AM (19YR-1F065), and the Armenian National Science and Education Fund based in New York, USA, to AM (ANSEF-NS-microbio-3869 and 4619).

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Margaryan, A., Panosyan, H., Birkeland, NK. (2021). Heavy Metal Resistance in Prokaryotes: Mechanism and Application. In: Egamberdieva, D., Birkeland, NK., Li, WJ., Panosyan, H. (eds) Microbial Communities and their Interactions in the Extreme Environment. Microorganisms for Sustainability, vol 32. Springer, Singapore. https://doi.org/10.1007/978-981-16-3731-5_13

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