[en] Competition shapes evolution. Toxic metals and metalloids have exerted selective pressure on life since the rise of the first organisms on the Earth, which has led to the evolution and acquisition of resistance mechanisms against them, as well as mechanisms to weaponize them. Microorganisms exploit antimicrobial metals and metalloids to gain competitive advantage over other members of microbial communities. This exerts a strong selective pressure that drives evolution of resistance. This review describes, with a focus on arsenic and copper, how microorganisms exploit metals and metalloids for predation and how metal- and metalloid-dependent predation may have been a driving force for evolution of microbial resistance against metals and metalloids.
Precision for document type :
Review article
Disciplines :
Environmental sciences & ecology
Author, co-author :
Li, Yuan Ping ✱; Institute of Environmental Microbiology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China, email: rensing@iue.ac.cn
Ben Fekih, Ibtissem ✱; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; Institute of Environmental Microbiology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China, email: rensing@iue.ac.cn
Chi Fru, Ernest; Centre for Geobiology and Geochemistry, School of Earth and Ocean Sciences, Cardiff University, CF10 3AT Cardiff, United Kingdom
Moraleda-Munoz, Aurelio; Departamento de Microbiología, Facultad de Ciencias, Universidad de Granada, Granada 18071, Spain
Li, Xuanji; Department of Biology, University of Copenhagen, DK-2200 Copenhagen, Denmark
Rosen, Barry P; Department of Cellular Biology and Pharmacology, Herbert Wertheim College of Medicine, Florida International University, Miami, Florida 33199, USA, email: myoshina@fiu.edu
Yoshinaga, Masafumi; Department of Cellular Biology and Pharmacology, Herbert Wertheim College of Medicine, Florida International University, Miami, Florida 33199, USA, email: myoshina@fiu.edu
Rensing, Christopher; Institute of Environmental Microbiology, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China, email: rensing@iue.ac.cn
✱ These authors have contributed equally to this work.
Our research was financially supported by grants from the National Natural Science Foundation of China (number 31770123) and the International Cooperation Science Foundation of Fujian Agriculture and Forestry University (number KXGH17013) to C.R., by NSF BIO/MCB grant 1817962 to M.Y., by NIH grants R35GM136211 and R01GM55425 to B.P.R., by European Research Council Grant 336092 to E.C.F., and by Spanish Government grants BFU2016-75425-P (70% funded by FEDER) and PID2020-112634GB-I00 to A.M.M.
Ahmad S,Lee SY,KongHG, Jo EJ, Choi HK, et al. 2016. Genetic determinants for pyomelanin production and its protective effect against oxidative stress in Ralstonia solanacearum. PLOS ONE 11:e0160845
Arguello JM, Patel SJ, Quintana J. 2016. Bacterial Cu+-ATPases: models for molecular structurefunction studies. Metallomics 8:906-14
Aurass P, Prager R, Flieger A. 2011. EHEC/EAEC O104:H4 strain linked with the 2011 German outbreak of haemolytic uremic syndrome enters into the viable but non-culturable state in response to various stresses and resuscitates upon stress relief. Environ.Microbiol. 13:3139-48
Ballabio C, Panagos P, Lugato E, Huang JH, Orgiazzi A, et al. 2018. Copper distribution in European top soils: an assessment based on Lucas soil survey. Sci. Total Environ. 636:282-98
Barber MF, Elde NC. 2015. Buried treasure: evolutionary perspectives on microbial iron piracy. Trends Genet. 31:627-36
Bitto NJ, Chapman R, Pidot S, Costin A, Lo C, et al. 2017. Bacterial membrane vesicles transport their DNA cargo into host cells. Sci. Rep. 7:7072
Bobrov A, Kirillina O, Fetherston J,Miller C, Burlison J, Perry R. 2014. The Yersinia pestis siderophore, yersiniabactin, and the ZnuABC system both contribute to zinc acquisition and the development of lethal septicemic plague in mice. Mol. Microbiol. 93(4):759-75
Braud A, Geoffroy V, Hoegy F,Mislin G, Schalk I. 2010. Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance. Environ.Microbiol. Rep. 2:419-25
Breuer C, Pichler T. 2013. Arsenic in marine hydrothermal fluids. Chem. Geol. 348:2-14
Budesinsky M, Budzikiewicz H, Prochazka Z, Ripperger H, Romer A, et al. 1980. Nicotianamine, a possible phytosiderophore of general occurrence. Phytochemistry 19:2295-97
Burckhardt RM, Escalante-Semerena JC. 2020. Small-molecule acetylation by GCN5-belated Nacetyltransferases in bacteria. Microbiol. Mol. Biol. Rev. 84:e00090-19
Callac N, Posth NR, Rattray JE, Yamoah KKY, Wiech A, et al. 2017. Modes of carbon fixation in an arsenic and CO2-rich shallow hydrothermal ecosystem. Sci. Rep. 7:14708
Caruana JC, Walper SA. 2020. Bacterial membrane vesicles as mediators of microbe-microbe and microbe-host community interactions. Front. Microbiol. 11:432
Casida LE. 1987. Relation to copper of N-1, a nonobligate bacterial predator. Appl. Environ. Microbiol. 53:1515-18
Casida LE. 1988. Minireview: nonobligate bacterial predation of bacteria in soil. Microb. Ecol. 15:1-8
Challenger F. 1951. Biological methylation. In Advances in Enzymology and Related Subjects of Biochemistry, ed. FF Nord, pp. 429-91. New York: Interscience
Chandrangsu P, Rensing C, Helmann J. 2017. Metal homeostasis and resistance in bacteria. Nat. Rev. Microbiol. 6:338-50
Chaturvedi KS, Hung CS, Crowley JR, Stapleton AE, Henderson JP. 2012. The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat. Chem. Biol. 8:731-36
Chaturvedi KS, Hung CS, Giblin DE, Urushidani S, Austin AM, et al. 2014. Cupric yersiniabactin is a virulence-associated superoxide dismutase mimic. ACS Chem. Biol. 9:551-61
Chauhan NS, Ranjan R, Purohit HJ, Kalia VC, Sharma R. 2009. Identification of genes conferring arsenic resistance to Escherichia coli from an effluent treatment plant sludge metagenomic library. FEMS Microbiol. Ecol. 67:130-39
Chen J, Bhattacharjee H, Rosen BP. 2015. ArsH is an organoarsenical oxidase that confers resistance to trivalent forms of the herbicide monosodium methylarsenate and the poultry growth promoter roxarsone. Mol. Microbiol. 96:1042-52
Chen J, Rosen BP. 2020. The Pseudomonas putida NfnB nitroreductase confers resistance to roxarsone. Sci. Total Environ. 748:141339
Chen J, Yoshinaga M, Rosen BP. 2019. The antibiotic action of methylarsenite is an emergent property of microbial communities. Mol. Microbiol. 111:487-94
Chen J, Zhang J, Rosen BP. 2019. Role of ArsEFG in roxarsone and nitarsone detoxification and resistance. Environ. Sci. Technol. 53:6182-91
Chen SC, Sun GX, Rosen BP, Zhang SY, Deng Y, et al. 2017. Recurrent horizontal transfer of arsenite methyltransferase genes facilitated adaptation of life to arsenic. Sci. Rep. 7:7741
Chen SC, Sun GX, Yan Y, Konstantinidis KT, Zhang SY, et al. 2020. The Great Oxidation Event expanded the genetic repertoire of arsenic metabolism and cycling. PNAS 117:10414-21
Chi Fru E, Arvestal E, Callac N, El Albani A, Kilias S, et al. 2015. Arsenic stress after the Proterozoic glaciations. Sci. Rep. 5:17789
Chi Fru E, Callac N, Posth NR, Argyraki A, Ling YC, et al. 2018. Arsenic and high affinity phosphate uptake gene distribution in shallow submarine hydrothermal sediments. Biogeochemistry 141:41-62
Chi Fru E, Ivarsson M, Kilias SP, Bengtson S, Belivanova V, et al. 2013. Fossilized iron bacteria reveal a pathway to the biological origin of banded iron formation. Nat. Commun. 4:2050
Chi Fru E, RodriguezNP, Partin CA,Lalonde SV, Andersson P, et al. 2016. Cu isotopes in marine black shales record the Great Oxidation Event. PNAS 113:4941-46
Chi Fru E, Somogyi A, El Albani A, Medjoubi K, Aubineau J, et al. 2019. The rise of oxygen-driven arsenic cycling at ca. 2.48 Ga. Geology 47:243-46
Choi DW, Semrau JD, AntholineWE, Hartsel SC, Anderson RC, et al. 2008. Oxidase, superoxide dismutase, and hydrogen peroxide reductase activities ofmethanobactin from types I and IImethanotrophs. J. Inorg. Biochem. 102:1571-80
Ciscato E, Bontognali T, Poulton S, Vance D. 2019. Copper and its isotopes in organic-rich sediments: from the modern Peru Margin to Archean shales. Geosciences 9:325
Clokie MRJ,Millard AD, Letarov AV, Heaphy S. 2011. Phages in nature. Bacteriophage 1:31-45
Cobine P, Cruz L, Navarrete F, Duncan D, Tygart M, Fuente L. 2013. Xylella fastidiosa differentially accumulates mineral elements in biofilm and planktonic cells. PLOS ONE 8:e54936
Contreras-Moreno FJ, Munoz-Dorado J, Garcia-Tomsig NI, Martinez-Navajas G, Perez J, Moraleda-Munoz A. 2020. Copper and melanin play a role in Myxococcus xanthus predation on Sinorhizobiummeliloti. Front. Microbiol. 11:94
Cordero RJ, Casadevall A. 2017. Functions of fungal melanin beyond virulence. Fungal Biol. Rev. 31:99-112
Cornu JY, Huguenot D, JezequelK,LollierM,LebeauT. 2017. Bioremediation of copper-contaminated soils by bacteria. J. Microbiol. Biotechnol. 33:26
Cornu JY, Randriamamonjy S, Gutierrez M, Rocco K, Gaudin P, et al. 2019. Copper phytoavailability in vineyard topsoils as affected by pyoverdine supply. Chemosphere 236:124347
Dassama LM, Kenney GE, Ro SY, Zielazinski EL, Rosenzweig AC. 2016. Methanobactin transport machinery. PNAS 113:13027-32
Deatherage BL, Cookson BT. 2012. Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect. Immun. 80:1948-57
DePas WH, Syed AK, Sifuentes M, Lee JS, Warshaw D, et al. 2014. Biofilm formation protects Escherichia coli against killing by Caenorhabditis elegans and Myxococcus xanthus. Appl. Environ. Microbiol. 80:7079-87
Diamond CW, Lyons TW. 2018. Mid-Proterozoic redox evolution and the possibility of transient oxygenation events. Emerg. Top. Life Sci. 2:235-45
Dinh TL, Akhmetova GR, Martykanova DS, Rudakova NL, Sharipova MR. 2019. Influence of divalent metal ions on biofilm formation by Bacillus subtilis. BioNanoScience 9:521-27
Djoko KY, Ong CY, Walker MJ, McEwan AG. 2015. The role of copper and zinc toxicity in innate immune defense against bacterial pathogens. J. Biol. Chem. 290:18954-61
Dupont CL, Grass G, Rensing C. 2011. Copper toxicity and the origin of bacterial resistance-new insights and applications. Metallomics 3:1109-18
Dwidjosiswojo Z,Richard J,Moritz MM,Dopp E, Flemming HC,Wingender J. 2011. Influence of copper ions on the viability and cytotoxicity of Pseudomonas aeruginosa under conditions relevant to drinking water environments. Int. J. Hyg. Environ. Health. 214:485-92
Ebrahim GJ. 2010. Bacterial resistance to antimicrobials. J. Trop. Pediatr. 56:141-143
Espinoza-Vergara G,Hoque MM, McDougald D, Noorian P. 2020. The impact of protozoan predation on the pathogenicity of Vibrio cholerae. Front. Microbiol. 11:17
Farhan Ul-Haque M, Kalidass B, Vorobev A, Baral BS,DiSpirito AA, Semrau JD. 2015. Methanobactin from Methylocystis sp. strain SB2 affects gene expression and methane monooxygenase activity in Methylosinus trichosporium OB3b. Appl. Environ.Microbiol. 81:2466-73
Garbinski LD, Rosen BP, Chen J. 2019. Pathways of arsenic uptake and efflux. Environ. Int. 126:585-97
Garbinski LD, Rosen BP, Yoshinaga M. 2020. Organoarsenicals inhibit bacterial peptidoglycan biosynthesis by targeting the essential enzyme MurA. Chemosphere 254:126911
German N, Doyscher D, Rensing C. 2013. Bacterial killing in macrophages and amoeba: Do they all use a brass dagger? Future Microbiol. 8:1257-64
Ghoul M, Mitri S. 2016. The ecology and evolution of microbial competition. Trends Microbiol. 24:833-45
Ghssein G, Brutesco C, Ouerdane L, Fojcik C, Izaute A, et al. 2016. Biosynthesis of a broad-spectrum nicotianamine-like metallophore in Staphylococcus aureus. Science 352:1105-9
Gibaud S, Jaouen G. 2010. Arsenic-based drugs: from Fowler's solution to modern anticancer chemotherapy. In Medicinal Organometallic Chemistry, ed. S Gibaud,G Jaouen, pp. 1-20. Berlin: Springer
Giovannoni SJ, Halsey KH, Saw J, Muslin O, Suffridge CP, et al. 2019. A parasitic arsenic cycle that shuttles energy from phytoplankton to heterotrophic bacterioplankton. mBio 10:e00246-19
Gomez-Santos N, Perez J, Sanchez-Sutil MC,Moraleda-Munoz A, Munoz-Dorado J. 2011. CorE from Myxococcus xanthus is a copper-dependent RNA polymerase sigma factor. PLOS Genet. 7:e1002106
Grinter R, Leung PM,Wijeyewickrema LC, Littler D, Beckham S, et al. 2019. Protease-associated import systems are widespread in Gram-negative bacteria. PLOS Genet. 15:e1008435
Haas H, Eisendle M, Turgeon BG. 2008. Siderophores in fungal physiology and virulence. Annu. Rev. Phytopathol. 46:149-87
Hakemian AS, Tinberg CE, Kondapalli KC, Telser J, Hoffman BM, et al. 2005. The copper chelator methanobactin from Methylosinus trichosporium OB3b binds copper(I). J. Am. Chem. Soc. 127:17142-43
Hao X, Luthje F, Ronn R, German NA, Li X, et al. 2016. A role for copper in protozoan grazing-two billion years selecting for bacterial copper resistance. Mol. Microbiol. 102:628-41
Harris T, Heidary N, Kozuch J, Frielingsdorf S, Lenz O, et al. 2018. In situ spectroelectrochemical studies into the formation and stability of robust diazonium-derived interfaces on gold electrodes for the immobilization of an oxygen-tolerant hydrogenase. ACS Appl. Mater. Interfaces 10:23380-91
Harrison JJ, Ceri H, Stremick CA, Turner RJ. 2004. Biofilm susceptibility to metal toxicity. Environ. Microbiol. 6:1220-27
Harrison JJ, Turner RJ, Ceri H. 2005. Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginosa. Environ.Microbiol. 7:981-94
Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35:322-32
Hsueh YH, Ke WJ, Hsieh CT, Lin KS, Tzou DY, Chiang CL. 2015. ZnO nanoparticles affect Bacillus subtilis cell growth and biofilm formation. PLOS ONE 10:e0128457
Jiang L. 2014. Low temperature and copper induce viable but nonculturable state of Salmonella typhi in the bottled drinking water. Adv. Mater. Res. 893:492-95
Johnston CW,Wyatt MA, Li X, Ibrahim A, Shuster J, et al. 2013. Gold biomineralization by a metallophore from a gold-associated microbe. Nat. Chem. Biol. 9:241-43
Keith KE, Killip L, He P, Moran GR, Valvano MA. 2007. Burkholderia cenocepacia C5424 produces a pigment with antioxidant properties using a homogentisate intermediate. J. Bacteriol. 189:9057-65
Kenney GE, Dassama LMK, Pandelia ME, Gizzi AS, Martinie RJ, et al. 2018. The biosynthesis of methanobactin. Science 359:1411-16
Kenney GE, Sadek M, Rosenzweig AC. 2016. Copper-responsive gene expression in the methanotroph Methylosinus trichosporium OB3b. Metallomics 8:931-40
Koh EI, Henderson JP. 2015. Microbial copper-binding siderophores at the host-pathogen interface. Aquat. Geochem. 290:18967-74
Kraemer SM, Duckworth OW, Harrington JM, SchenkeveldWD. 2015. Metallophores and trace metal biogeochemistry. Aquat. Geochem. 21:159-95
Kritharis A, Bradley TP, Budman DR. 2013. The evolving use of arsenic in pharmacotherapy of malignant disease. Ann. Hematol. 92:719-30
Kuramata M, Sakakibara F, Kataoka R, Yamazaki K, Baba K, et al. 2016. Arsinothricin, a novel organoarsenic species produced by a rice rhizosphere bacterium. Environ. Chem. 13(4):723-31
Ladomersky E, Petris MJ. 2015. Copper tolerance and virulence in bacteria. Metallomics 7:957-64
Li LG, Xia Y, Zhang T. 2017. Co-occurrence of antibiotic and metal resistance genes revealed in complete genome collection. ISME J. 11:651-62
Lichtmannegger J, Leitzinger C,Wimmer R, Schmitt S, Schulz S, et al. 2016. Methanobactin reverses acute liver failure in a rat model ofWilson disease. J. Microbiol. Immunol. Infect. 126:2721-35
Lin WP, Lai HL, Liu YL, Chiung YM, Shiau CY, et al. 2005. Effect of melanin produced by a recombinant Escherichia coli on antibacterial activity of antibiotics. J. Microbiol. Immunol. Infect. 38:320-26
Lonetto MA, Donohue TJ, Gross CA, Buttner MJ. 2019. Discovery of the extracytoplasmic function σ factors. Mol. Microbiol. 112:348-55
LyonsTW,Reinhard CT,PlanavskyNJ. 2014.The rise of oxygen in Earth's early ocean and atmosphere. Nature 506:307-15
Makkar NS, Casida LE. 1987.Technique for estimating low numbers of a bacterial strain(s) in soil. Appl. Environ.Microbiol. 53:887-88
Mangalgiri KP, Adak A, Blaney L. 2015. Organoarsenicals in poultry litter: detection, fate, and toxicity. Environ. Int. 75:68-80
Marcos-Torres FJ, Perez J, Gomez-Santos N, Moraleda-Munoz A, Munoz-Dorado J. 2016. In depth analysis of the mechanism of action of metal-dependent sigma factors: characterization of CorE2 from Myxococcus xanthus. Nucleic. Acids. Res. 44:5571-84
Mashburn LM, Whiteley M. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422-25
Moore EK, Jelen BI, Giovannelli D, Raanan H,Falkowski PG. 2017. Metal availability and the expanding network of microbial metabolisms in the Archaean eon. Nat. Geosci. 10:629-36
Moraleda-Munoz A, Marcos-Torres FJ, Perez J, Munoz-Dorado J. 2019. Metal-responsive RNA polymerase extracytoplasmic function (ECF) sigma factors. Mol. Microbiol. 112:385-98
Moraleda-Munoz A, Perez J, Extremera AL, Munoz-Dorado J. 2010. Differential regulation of six heavy metal efflux systems in the response of Myxococcus xanthus to copper. Appl. Environ.Microbiol. 76:6069-76
Moraleda-Munoz A, Perez J, Extremera AL, Munoz-Dorado J. 2010. Expression and physiological role of three Myxococcus xanthus copper-dependent P1B-type ATPases during bacterial growth and development. Appl. Environ.Microbiol. 76:6077-84
Mozzi A, Forni D, Clerici M, Cagliani R, Sironi M. 2018. The diversity of mammalian hemoproteins and microbial heme scavengers is shaped by an arms race for iron piracy. Front. Immunol. 9:2086
Muller S, Strack SN, Hoefler BC, Straight PD, Kearns DB, Kirby JR. 2014. Bacillaene and sporulation protect Bacillus subtilis from predation by Myxococcus xanthus. Appl. Environ.Microbiol. 80:5603-10
Muller S, Strack SN, Ryan SE, Kearns DB, Kirby JR. 2015. Predation by Myxococcus xanthus induces Bacillus subtilis to form spore-filled megastructures. Appl. Environ.Microbiol. 81:203-10
Munita JM, Arias CA. 2016. Mechanisms of antibiotic resistance. Microbiol. Spectr. 4:10
Muranaka LS,TakitaMA, Olivato JC, Kishi LT, de Souza AA. 2012. Global expression profile of biofilm resistance to antimicrobial compounds in the plant-pathogenic bacterium Xylella fastidiosa reveals evidence of persister cells J. Bacteriol. 194:4561-69
Nadar VS, Chen J, Dheeman DS,Galvan AE,Yoshinaga-SakuraiK, et al. 2019. Arsinothricin, an arseniccontaining non-proteinogenic amino acid analog of glutamate, is a broad-spectrum antibiotic. Commun. Biol. 2:131
Nair RR, Vasse M,Wielgoss S, Sun L, Yu Y-TN, Velicer GJ. 2019. Bacterial predator-prey coevolution accelerates genome evolution and selects on virulence-associated prey defences. Nat. Commun. 10:4301
Narbonne GM. 2004. The Ediacara biota: neoproterozoic origin of animals and their ecosystems. Annu. Rev. Earth. Planet. Sci. 33:421-42
Nies DH. 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27:313-39
Nolan EM. 2017. A noncanonical role for yersiniabactin in bacterial copper acquisition. Biochemistry 56:6073-74
Page K,Wilson M, Parkin IP. 2009. Antimicrobial surfaces and their potential in reducing the role of the inanimate environment in the incidence of hospital-acquired infections. J. Mater. Chem. 19:3819-31
Pal C, Asiani K, Arya S, Rensing C, Stekel DJ, et al. 2017. Metal resistance and its association with antibiotic resistance. Adv. Microb. Physiol. 70:261-313
Papkou A, Guzella T,Yang W,Koepper S,Pees B, et al. 2019.The genomic basis of Red Queen dynamics during rapid reciprocal host-pathogen coevolution. PNAS 116:923-28
Parker DL, Lee SW, Geszvain K, Davis RE, Gruffaz C, et al. 2014. Pyoverdine synthesis by the Mn(II)-oxidizing bacterium Pseudomonas putida GB-1. Front. Microbiol. 5:202
Pavan ME, Lopez NI, Pettinari MJ. 2020. Melanin biosynthesis in bacteria, regulation and production perspectives. Appl.Microbiol. Biotechnol. 104:1357-70
Pavan ME, Pavan EE, Lopez NI, Levin L, Pettinari MJ. 2015. Living in an extremely polluted environment: clues from the genome of melanin-producing Aeromonas salmonicida subsp. pectinolytica 34melT. Appl. Environ.Microbiol. 81:5235-48
Perez J, Jimenez-Zurdo JI, Martinez-Abarca F,Millan V, Shimkets LJ,Munoz-Dorado J. 2014. Rhizobial galactoglucan determines the predatory pattern of Myxococcus xanthus and protects Sinorhizobium meliloti from predation. Environ.Microbiol. 16:2341-50
Perez J, Munoz-Dorado J, Moraleda-Munoz A. 2018. The complex global response to copper in the multicellular bacterium Myxococcus xanthus.Metallomics 10:876-86
Poole K. 2017. At the nexus of antibiotics and metals: the impact of Cu and Zn on antibiotic activity and resistance. Trends Microbiol. 25:820-32
Poulton SW, Canfield DE. 2011. Ferruginous conditions: a dominant feature of the ocean through Earth's history. Elements 7:107-12
Rademacher C, Masepohl B. 2012. Copper-responsive gene regulation in bacteria. Microbiology 158:2451-64
Rascovan N, Maldonado J, Vazquez MP, Farias ME. 2016. Metagenomic study of red biofilms from Diamante Lake reveals ancient arsenic bioenergetics in haloarchaea. ISME J. 10:299-309
Raymond KN, Allred BE, Sia AK. 2015. Coordination chemistry of microbial iron transport. Accounts Chem. Res. 48:2496-505
Rensing C,Moodley A, Cavaco LM,McDevitt SF. 2018. Resistance to metals used in agricultural production. Microbiol. Spectr. 6(2). https://doi.org/10.1128/microbiolspec.ARBA-0025-2017
Ridge PG, Zhang Y, Gladyshev VN. 2008. Comparative genomic analyses of copper transporters and cuproproteomes reveal evolutionary dynamics of copper utilization and its link to oxygen. PLOS ONE 3:e1378
Robbins LJ, Lalonde SV, Planavsky NJ, Partin CA, Reinhard CT, et al. 2016. Trace elements at the intersection of marine biological and geochemical evolution. Earth-Sci. Rev. 163:323-48
Robinson NJ,Winge DR. 2010. Copper metallochaperones. Annu. Rev. Biochem. 79:537-62
RutherfordDW,Bednar AJ, Garbarino JR,Needham R, Staver KW,Wershaw RL. 2003. Environmental fate of roxarsone in poultry litter. Part II. Mobility of arsenic in soils amended with poultry litter. Environ. Sci. Technol. 37:1515-20
Sanchez-SutilMC, Gomez-Santos N,Moraleda-Munoz A, Martins LO,Perez J,Munoz-Dorado J. 2007. Differential expression of the three multicopper oxidases from Myxococcus xanthus. J. Bacteriol. 189:4887-98
Sanchez-SutilMC, Marcos-Torres FJ, Perez J,Ruiz-GonzalezM,Garcia-Bravo E, et al. 2016. Dissection of the sensor domain of the copper-responsive histidine kinase CorS from Myxococcus xanthus. Environ. Microbiol. Rep. 8:363-70
Sanchez-Sutil MC, Perez J, Gomez-Santos N, Shimkets LJ, Moraleda-Munoz A, Munoz-Dorado J. 2013. The Myxococcus xanthus two-component system CorSR regulates expression of a gene cluster involved in maintaining copper tolerance during growth and development. PLOS ONE 8:e68240
Sancho-Tomas M, Somogyi A,Medjoubi K, Bergamaschi A,Visscher PT, et al. 2018. Distribution, redox state and (bio)geochemical implications of arsenic in present day microbialites of Laguna Brava, Salar de Atacama. Chem. Geol. 490:13-21
Sanders OI, Rensing C, Kuroda M, Mitra B, Rosen BP. 1997. Antimonite is accumulated by the glycerol facilitator GlpF in Escherichia coli. J. Bacteriol. 179:3365-67
Schmidt MG, von Dessauer B, Benavente C, Benadof D, Cifuentes P, et al. 2016. Copper surfaces are associated with significantly lower concentrations of bacteria on selected surfaces within a pediatric intensive care unit. Am. J. Infect. Control 44:203-9
Seccareccia I, Kovacs AT, Gallegos-Monterrosa R, Nett M. 2016. Unraveling the predator-prey relationship of Cupriavidus necator and Bacillus subtilis. Microbiol. Res. 192:231-38
Seiler C, Berendonk TU. 2012. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front. Microbiol. 3:399
Shi K, Li C, Rensing C, Dai X, Fan X,Wang G. 2018. Efflux transporter ArsK is responsible for bacterial resistance to arsenite, antimonite, trivalent roxarsone, and methylarsenite. Appl. Environ. Microbiol. 84:e01842-18
Sirelkhatim A,Mahmud S, Seeni A, KausNHM,Ann LC, et al. 2015. Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nano-Micro. Lett. 7:219-42
Sun S,Noorian P, McDougald D. 2018. Dual role of mechanisms involved in resistance to predation by protozoa and virulence to humans. Front. Microbiol. 9:1017
Taylor V, Goodale B, Raab A, Schwerdtle T, Reimer K, et al. 2017. Human exposure to organic arsenic species from seafood. Sci. Total Environ. 580:266-82
Teitzel GM, Parsek MR. 2003. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ.Microbiol. 69:2313-20
Tella M, Bravin MN, Thuries L, Cazevieille P, Chevassus-Rosset C, et al. 2016. Increased zinc and copper availability in organic waste amended soil potentially involving distinct release mechanisms. Environ. Pollut. 212:299-306
Thery C, Ostrowski M, Segura E. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9:581-93
Tokmina-LukaszewskaM, Shi Z,Tripet B, McDermott TR, Copie V, et al. 2017. Metabolic response of Agrobacterium tumefaciens 5A to arsenite. Environ.Microbiol. 19:710-21
Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. 2012. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol. Microbiol. 86:628-44
Vincent M, Duval R, Hartemann P, Engels-Deutsch M. 2018. Contact killing and antimicrobial properties of copper. J. Appl.Microbiol. 124:1032-46
Vorobev A, Jagadevan S, Baral BS, DiSpirito AA, Freemeier BC, et al. 2013. Detoxification of mercury by methanobactin from Methylosinus trichosporium OB3b. Appl. Environ.Microbiol. 79:5918
Waksman SA. 1947. What is an antibiotic or an antibiotic substance? Mycologia 39:565-69
Wichard T, Mishra B, Myneni SCB, Bellenger JP, Kraepiel AM. 2009. Storage and bioavailability of molybdenum in soils increased by organic matter complexation. Nat. Geosci. 2:625-29
Wright PM, Seiple IB, Myers AG. 2014. The evolving role of chemical synthesis in antibacterial drug discovery. Angew. Chem. Int. Edit. Engl. 53:8840-69
Xin JY, Lin K,Wang Y, Xia CG. 2014. Methanobactin-mediated synthesis of gold nanoparticles supported over Al2O3 toward an efficient catalyst for glucose oxidation. Int. J. Mol. Sci. 15:21603-20
Xue XM, Ye J, Raber G, Rosen BP, Francesconi K, et al. 2019. Identification of steps in the pathway of arsenosugar biosynthesis. Environ. Sci. Technol. 53:634-41
Yan Y, Chen J,Galvan AE, Garbinski LD, Zhu YG, et al. 2019. Reduction of organoarsenical herbicides and antimicrobial growth promoters by the legume symbiont Sinorhizobium meliloti. Environ. Sci. Technol. 53:13648-56
Yang HC, Rosen BP. 2016. New mechanisms of bacterial arsenic resistance. Biomed. J. 39:5-13
Yang Z, Peng H, Lu X, Liu Q,Huang R, et al. 2016. Arsenic metabolites, including N-acetyl-4-hydroxym-arsanilic acid, in chicken litter from a roxarsone-feeding study involving 1600 chickens. Environ. Sci. Technol. 50:6737-43
Yoshinaga M, Cai Y, Rosen BP. 2011. Demethylation of methylarsonic acid by a microbial community. Environ.Microbiol. 13:1205-15
Yoshinaga M, Rosen BP. 2014. A CAs lyase for degradation of environmental organoarsenical herbicides and animal husbandry growth promoters. PNAS 111:7701-6
Young CA, Gordon LD, Fang Z, Holder RC, Reid SD. 2015. Copper tolerance and characterization of a copper-responsive operon, copYAZ, in an M1T1 clinical strain of Streptococcus pyogenes. J. Bacteriol. 197:2580-92
Zeph LR, Casida LE Jr. 1986. Gram-negative versus gram-positive (actinomycete) nonobligate bacterial predators of bacteria in soil. Appl. Environ.Microbiol. 52:819-23
Zhang X, Li B, Deng J, Qin B, Wells M, Tefsen B. 2020. Quantitative high-throughput approach to chalkophore screening in freshwaters. Sci. Total Environ. 735:139476
