1932

Abstract

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.

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2021-10-08
2024-03-29
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Literature Cited

  1. 1. 
    Ahmad S, Lee SY, Kong HG, 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
    [Google Scholar]
  2. 2. 
    Argüello JM, Patel SJ, Quintana J. 2016. Bacterial Cu+-ATPases: models for molecular structure-function studies. Metallomics 8:906–14
    [Google Scholar]
  3. 3. 
    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
    [Google Scholar]
  4. 4. 
    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
    [Google Scholar]
  5. 5. 
    Barber MF, Elde NC. 2015. Buried treasure: evolutionary perspectives on microbial iron piracy. Trends Genet 31:627–36
    [Google Scholar]
  6. 6. 
    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
    [Google Scholar]
  7. 7. 
    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. 93:4759–75
    [Google Scholar]
  8. 8. 
    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
    [Google Scholar]
  9. 9. 
    Breuer C, Pichler T. 2013. Arsenic in marine hydrothermal fluids. Chem. Geol. 348:2–14
    [Google Scholar]
  10. 10. 
    Buděšínský M, Budzikiewicz H, Procházka Ž, Ripperger H, Römer A et al. 1980. Nicotianamine, a possible phytosiderophore of general occurrence. Phytochemistry 19:2295–97
    [Google Scholar]
  11. 11. 
    Burckhardt RM, Escalante-Semerena JC. 2020. Small-molecule acetylation by GCN5-belated N-acetyltransferases in bacteria. Microbiol. Mol. Biol. Rev. 84:e00090-19
    [Google Scholar]
  12. 12. 
    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
    [Google Scholar]
  13. 13. 
    Caruana JC, Walper SA. 2020. Bacterial membrane vesicles as mediators of microbe-microbe and microbe-host community interactions. Front. Microbiol. 11:432
    [Google Scholar]
  14. 14. 
    Casida LE. 1987. Relation to copper of N-1, a nonobligate bacterial predator. Appl. Environ. Microbiol. 53:1515–18
    [Google Scholar]
  15. 15. 
    Casida LE. 1988. Minireview: nonobligate bacterial predation of bacteria in soil. Microb. Ecol. 15:1–8
    [Google Scholar]
  16. 16. 
    Challenger F. 1951. Biological methylation. Advances in Enzymology and Related Subjects of Biochemistry FF Nord 429–91 New York: Interscience
    [Google Scholar]
  17. 17. 
    Chandrangsu P, Rensing C, Helmann J. 2017. Metal homeostasis and resistance in bacteria. Nat. Rev. Microbiol. 6:338–50
    [Google Scholar]
  18. 18. 
    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
    [Google Scholar]
  19. 19. 
    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
    [Google Scholar]
  20. 20. 
    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
    [Google Scholar]
  21. 21. 
    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
    [Google Scholar]
  22. 22. 
    Chen J, Rosen BP. 2020. The Pseudomonas putida NfnB nitroreductase confers resistance to roxarsone. Sci. Total Environ. 748:141339
    [Google Scholar]
  23. 23. 
    Chen J, Yoshinaga M, Rosen BP. 2019. The antibiotic action of methylarsenite is an emergent property of microbial communities. Mol. Microbiol. 111:487–94
    [Google Scholar]
  24. 24. 
    Chen J, Zhang J, Rosen BP. 2019. Role of ArsEFG in roxarsone and nitarsone detoxification and resistance. Environ. Sci. Technol. 53:6182–91
    [Google Scholar]
  25. 25. 
    Chen L, Valentine JL, Huang CJ, Endicott CE, Moeller TD et al. 2016. Outer membrane vesicles displaying engineered glycotopes elicit protective antibodies. PNAS 113:E3609–18
    [Google Scholar]
  26. 26. 
    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
    [Google Scholar]
  27. 27. 
    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
    [Google Scholar]
  28. 28. 
    Chi Fru E, Arvestål E, Callac N, El Albani A, Kilias S et al. 2015. Arsenic stress after the Proterozoic glaciations. Sci. Rep. 5:17789
    [Google Scholar]
  29. 29. 
    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
    [Google Scholar]
  30. 30. 
    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
    [Google Scholar]
  31. 31. 
    Chi Fru E, Rodríguez NP, Partin CA, Lalonde SV, Andersson P et al. 2016. Cu isotopes in marine black shales record the Great Oxidation Event. PNAS 113:4941–46
    [Google Scholar]
  32. 32. 
    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
    [Google Scholar]
  33. 33. 
    Choi DW, Semrau JD, Antholine WE, Hartsel SC, Anderson RC et al. 2008. Oxidase, superoxide dismutase, and hydrogen peroxide reductase activities of methanobactin from types I and II methanotrophs. J. Inorg. Biochem. 102:1571–80
    [Google Scholar]
  34. 34. 
    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
    [Google Scholar]
  35. 35. 
    Clokie MRJ, Millard AD, Letarov AV, Heaphy S. 2011. Phages in nature. Bacteriophage 1:31–45
    [Google Scholar]
  36. 36. 
    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
    [Google Scholar]
  37. 37. 
    Contreras-Moreno FJ, Muñoz-Dorado J, García-Tomsig NI, Martínez-Navajas G, Pérez J, Moraleda-Muñoz A. 2020. Copper and melanin play a role in Myxococcus xanthus predation on Sinorhizobium meliloti. Front. Microbiol. 11:94
    [Google Scholar]
  38. 38. 
    Cordero RJ, Casadevall A. 2017. Functions of fungal melanin beyond virulence. Fungal Biol. Rev. 31:99–112
    [Google Scholar]
  39. 39. 
    Cornu JY, Huguenot D, Jézéquel K, Lollier M, Lebeau T. 2017. Bioremediation of copper-contaminated soils by bacteria. J. Microbiol. Biotechnol. 33:26
    [Google Scholar]
  40. 40. 
    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
    [Google Scholar]
  41. 41. 
    Dassama LM, Kenney GE, Ro SY, Zielazinski EL, Rosenzweig AC 2016. Methanobactin transport machinery. PNAS 113:13027–32
    [Google Scholar]
  42. 42. 
    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
    [Google Scholar]
  43. 43. 
    Delmar JA, Su CC, Yu EW. 2014. Bacterial multidrug efflux transporters. Annu. Rev. Biophys. 43:93–117
    [Google Scholar]
  44. 44. 
    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
    [Google Scholar]
  45. 45. 
    Diamond CW, Lyons TW. 2018. Mid-Proterozoic redox evolution and the possibility of transient oxygenation events. Emerg. Top. Life Sci. 2:235–45
    [Google Scholar]
  46. 46. 
    Dinh ТL, Akhmetova GR, Martykanova DS, Rudakova NL, Sharipova МR. 2019. Influence of divalent metal ions on biofilm formation by Bacillus subtilis. BioNanoScience 9:521–27
    [Google Scholar]
  47. 47. 
    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
    [Google Scholar]
  48. 48. 
    Dupont CL, Grass G, Rensing C. 2011. Copper toxicity and the origin of bacterial resistance—new insights and applications. Metallomics 3:1109–18
    [Google Scholar]
  49. 49. 
    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
    [Google Scholar]
  50. 50. 
    Ebrahim GJ. 2010. Bacterial resistance to antimicrobials. J. Trop. Pediatr. 56:141–143
    [Google Scholar]
  51. 51. 
    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
    [Google Scholar]
  52. 52. 
    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
    [Google Scholar]
  53. 53. 
    Garbinski LD, Rosen BP, Chen J 2019. Pathways of arsenic uptake and efflux. Environ. Int. 126:585–97
    [Google Scholar]
  54. 54. 
    Garbinski LD, Rosen BP, Yoshinaga M. 2020. Organoarsenicals inhibit bacterial peptidoglycan biosynthesis by targeting the essential enzyme MurA. Chemosphere 254:126911
    [Google Scholar]
  55. 55. 
    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
    [Google Scholar]
  56. 56. 
    Ghoul M, Mitri S. 2016. The ecology and evolution of microbial competition. Trends Microbiol 24:833–45
    [Google Scholar]
  57. 57. 
    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
    [Google Scholar]
  58. 58. 
    Gibaud S, Jaouen G 2010. Arsenic-based drugs: from Fowler's solution to modern anticancer chemotherapy. Medicinal Organometallic Chemistry S Gibaud, G Jaouen pp. 120 Berlin: Springer
    [Google Scholar]
  59. 59. 
    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
    [Google Scholar]
  60. 60. 
    Gómez-Santos N, Pérez J, Sánchez-Sutil MC, Moraleda-Muñoz A, Muñoz-Dorado J. 2011. CorE from Myxococcus xanthus is a copper-dependent RNA polymerase sigma factor. PLOS Genet 7:e1002106
    [Google Scholar]
  61. 61. 
    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
    [Google Scholar]
  62. 62. 
    Haas H, Eisendle M, Turgeon BG. 2008. Siderophores in fungal physiology and virulence. Annu. Rev. Phytopathol. 46:149–87
    [Google Scholar]
  63. 63. 
    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
    [Google Scholar]
  64. 64. 
    Hao X, Lüthje F, Rønn 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
    [Google Scholar]
  65. 65. 
    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
    [Google Scholar]
  66. 66. 
    Harrison JJ, Ceri H, Stremick CA, Turner RJ. 2004. Biofilm susceptibility to metal toxicity. Environ. Microbiol. 6:1220–27
    [Google Scholar]
  67. 67. 
    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
    [Google Scholar]
  68. 68. 
    Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. 2010. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35:322–32
    [Google Scholar]
  69. 69. 
    Horsman GP, Zechel DL. 2017. Phosphonate biochemistry. Chem. Rev. 117:5704–83
    [Google Scholar]
  70. 70. 
    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
    [Google Scholar]
  71. 71. 
    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
    [Google Scholar]
  72. 72. 
    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
    [Google Scholar]
  73. 73. 
    Johnstone TC, Nolan EM. 2015. Beyond iron: non-classical biological functions of bacterial siderophores. Dalton. Trans. 44:6320–39
    [Google Scholar]
  74. 74. 
    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
    [Google Scholar]
  75. 75. 
    Kenney GE, Dassama LMK, Pandelia ME, Gizzi AS, Martinie RJ et al. 2018. The biosynthesis of methanobactin. Science 359:1411–16
    [Google Scholar]
  76. 76. 
    Kenney GE, Rosenzweig AC. 2013. Genome mining for methanobactins. BMC Biol 11:17
    [Google Scholar]
  77. 77. 
    Kenney GE, Rosenzweig AC. 2018. Chalkophores. Annu. Rev. Biochem. 87:645–76
    [Google Scholar]
  78. 78. 
    Kenney GE, Sadek M, Rosenzweig AC. 2016. Copper-responsive gene expression in the methanotroph Methylosinus trichosporium OB3b. Metallomics 8:931–40
    [Google Scholar]
  79. 79. 
    Koh EI, Henderson JP. 2015. Microbial copper-binding siderophores at the host-pathogen interface. Aquat. Geochem. 290:18967–74
    [Google Scholar]
  80. 80. 
    Kraemer SM, Duckworth OW, Harrington JM, Schenkeveld WD. 2015. Metallophores and trace metal biogeochemistry. Aquat. Geochem. 21:159–95
    [Google Scholar]
  81. 81. 
    Kritharis A, Bradley TP, Budman DR. 2013. The evolving use of arsenic in pharmacotherapy of malignant disease. Ann. Hematol. 92:719–30
    [Google Scholar]
  82. 82. 
    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. 13:4723–31
    [Google Scholar]
  83. 83. 
    Ladomersky E, Petris MJ. 2015. Copper tolerance and virulence in bacteria. Metallomics 7:957–64
    [Google Scholar]
  84. 84. 
    Lankford CE, Byers BR. 1973. Bacterial assimilation of iron. CRC Crit. Rev. Microbiol. 2:273–331
    [Google Scholar]
  85. 85. 
    Large RR, Mukherjee I, Gregory D, Steadman J, Corkrey R, Danyushevsky LV 2019. Atmosphere oxygen cycling through the Proterozoic and Phanerozoic. Miner. Depos 54:485–506
    [Google Scholar]
  86. 86. 
    Large RR 2020. Evolution of Earth's atmosphere. Encyclopedia of Geology S Elias, D Alderton Amsterdam: Elsevier, 2nd ed..
    [Google Scholar]
  87. 87. 
    Lemire JA, Harrison JJ, Turner RJ. 2013. Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat. Rev. Microbiol. 11:371–84
    [Google Scholar]
  88. 88. 
    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
    [Google Scholar]
  89. 89. 
    Lichtmannegger J, Leitzinger C, Wimmer R, Schmitt S, Schulz S et al. 2016. Methanobactin reverses acute liver failure in a rat model of Wilson disease. J. Microbiol. Immunol. Infect. 126:2721–35
    [Google Scholar]
  90. 90. 
    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
    [Google Scholar]
  91. 91. 
    Lonetto MA, Donohue TJ, Gross CA, Buttner MJ. 2019. Discovery of the extracytoplasmic function σ factors. Mol. Microbiol. 112:348–55
    [Google Scholar]
  92. 92. 
    Lyons TW, Reinhard CT, Planavsky NJ. 2014. The rise of oxygen in Earth's early ocean and atmosphere. Nature 506:307–15
    [Google Scholar]
  93. 93. 
    Makkar NS, Casida LE. 1987. Technique for estimating low numbers of a bacterial strain(s) in soil. Appl. Environ. Microbiol. 53:887–88
    [Google Scholar]
  94. 94. 
    Mangalgiri KP, Adak A, Blaney L. 2015. Organoarsenicals in poultry litter: detection, fate, and toxicity. Environ. Int. 75:68–80
    [Google Scholar]
  95. 95. 
    Marcos-Torres FJ, Pérez J, Gómez-Santos N, Moraleda-Muñoz A, Muñoz-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
    [Google Scholar]
  96. 96. 
    Mashburn LM, Whiteley M. 2005. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422–25
    [Google Scholar]
  97. 97. 
    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
    [Google Scholar]
  98. 98. 
    Moraleda-Muñoz A, Marcos-Torres FJ, Pérez J, Muñoz-Dorado J 2019. Metal-responsive RNA polymerase extracytoplasmic function (ECF) sigma factors. Mol. Microbiol. 112:385–98
    [Google Scholar]
  99. 99. 
    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. 76:6069–76
    [Google Scholar]
  100. 100. 
    Moraleda-Muñoz A, Pérez J, Extremera AL, Muñoz-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
    [Google Scholar]
  101. 101. 
    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
    [Google Scholar]
  102. 102. 
    Mukhopadhyay R, Bhattacharjee H, Rosen BP. 2014. Aquaglyceroporins: generalized metalloid channels. Biochim. Biophys. Acta Gen. Subj. 1840:1583–91
    [Google Scholar]
  103. 103. 
    Müller 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
    [Google Scholar]
  104. 104. 
    Müller 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
    [Google Scholar]
  105. 105. 
    Munita JM, Arias CA. 2016. Mechanisms of antibiotic resistance. Microbiol. Spectr. 4:10
    [Google Scholar]
  106. 106. 
    Muranaka LS, Takita MA, 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
    [Google Scholar]
  107. 107. 
    Nadar VS, Chen J, Dheeman DS, Galván AE, Yoshinaga-Sakurai K et al. 2019. Arsinothricin, an arsenic-containing non-proteinogenic amino acid analog of glutamate, is a broad-spectrum antibiotic. Commun. Biol. 2:131
    [Google Scholar]
  108. 108. 
    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
    [Google Scholar]
  109. 109. 
    Narbonne GM. 2004. The Ediacara biota: neoproterozoic origin of animals and their ecosystems. Annu. Rev. Earth. Planet. Sci. 33:421–42
    [Google Scholar]
  110. 110. 
    Nies DH. 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27:313–39
    [Google Scholar]
  111. 111. 
    Nolan EM. 2017. A noncanonical role for yersiniabactin in bacterial copper acquisition. Biochemistry 56:6073–74
    [Google Scholar]
  112. 112. 
    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
    [Google Scholar]
  113. 113. 
    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
    [Google Scholar]
  114. 114. 
    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
    [Google Scholar]
  115. 115. 
    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
    [Google Scholar]
  116. 116. 
    Pavan ME, Lopez NI, Pettinari MJ. 2020. Melanin biosynthesis in bacteria, regulation and production perspectives. Appl. Microbiol. Biotechnol. 104:1357–70
    [Google Scholar]
  117. 117. 
    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
    [Google Scholar]
  118. 118. 
    Pérez J, Jiménez-Zurdo JI, Martínez-Abarca F, Millán V, Shimkets LJ, Muñoz-Dorado J. 2014. Rhizobial galactoglucan determines the predatory pattern of Myxococcus xanthus and protects Sinorhizobium meliloti from predation. Environ. Microbiol. 16:2341–50
    [Google Scholar]
  119. 119. 
    Pérez J, Muñoz-Dorado J, Moraleda-Muñoz A. 2018. The complex global response to copper in the multicellular bacterium Myxococcus xanthus. Metallomics 10:876–86
    [Google Scholar]
  120. 120. 
    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
    [Google Scholar]
  121. 121. 
    Poulton SW, Canfield DE. 2011. Ferruginous conditions: a dominant feature of the ocean through Earth's history. Elements 7:107–12
    [Google Scholar]
  122. 122. 
    Rademacher C, Masepohl B. 2012. Copper-responsive gene regulation in bacteria. Microbiology 158:2451–64
    [Google Scholar]
  123. 123. 
    Radke B, Jewell L, Piketh S, Namieśnik J. 2014. Arsenic-based warfare agents: production, use, and destruction. Crit. Rev. Environ. Sci. Technol. 44:1525–76
    [Google Scholar]
  124. 124. 
    Rascovan N, Maldonado J, Vazquez MP, Farías ME. 2016. Metagenomic study of red biofilms from Diamante Lake reveals ancient arsenic bioenergetics in haloarchaea. ISME J 10:299–309
    [Google Scholar]
  125. 125. 
    Raymond KN, Allred BE, Sia AK. 2015. Coordination chemistry of microbial iron transport. Accounts Chem. Res. 48:2496–505
    [Google Scholar]
  126. 126. 
    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
    [Crossref] [Google Scholar]
  127. 127. 
    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
    [Google Scholar]
  128. 128. 
    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
    [Google Scholar]
  129. 129. 
    Robinson NJ, Winge DR. 2010. Copper metallochaperones. Annu. Rev. Biochem. 79:537–62
    [Google Scholar]
  130. 130. 
    Rutherford DW, 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
    [Google Scholar]
  131. 131. 
    Sánchez-Sutil MC, Gómez-Santos N, Moraleda-Muñoz A, Martins LO, Pérez J, Muñoz-Dorado J. 2007. Differential expression of the three multicopper oxidases from Myxococcus xanthus. J. Bacteriol. 189:4887–98
    [Google Scholar]
  132. 132. 
    Sánchez-Sutil MC, Marcos-Torres FJ, Pérez J, Ruiz-González M, García-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
    [Google Scholar]
  133. 133. 
    Sánchez-Sutil MC, Pérez J, Gómez-Santos N, Shimkets LJ, Moraleda-Muñoz A, Muñoz-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
    [Google Scholar]
  134. 134. 
    Sancho-Tomás 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
    [Google Scholar]
  135. 135. 
    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
    [Google Scholar]
  136. 136. 
    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
    [Google Scholar]
  137. 137. 
    Seccareccia I, Kovács ÁT, Gallegos-Monterrosa R, Nett M. 2016. Unraveling the predator-prey relationship of Cupriavidus necator and Bacillus subtilis. Microbiol. Res. 192:231–38
    [Google Scholar]
  138. 138. 
    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
    [Google Scholar]
  139. 139. 
    Deleted in proof
  140. 140. 
    Shen S, Li XF, Cullen WR, Weinfeld M, Le XC. 2013. Arsenic binding to proteins. Chem. Rev. 113:7769–92
    [Google Scholar]
  141. 141. 
    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
    [Google Scholar]
  142. 142. 
    Sirelkhatim A, Mahmud S, Seeni A, Kaus NHM, Ann LC et al. 2015. Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nano-Micro. Lett 7:219–42
    [Google Scholar]
  143. 143. 
    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
    [Google Scholar]
  144. 144. 
    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
    [Google Scholar]
  145. 145. 
    Teitzel GM, Parsek MR. 2003. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 69:2313–20
    [Google Scholar]
  146. 146. 
    Tella M, Bravin MN, Thuriès 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
    [Google Scholar]
  147. 147. 
    Théry C, Ostrowski M, Segura E. 2009. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9:581–93
    [Google Scholar]
  148. 148. 
    Tokmina-Lukaszewska M, Shi Z, Tripet B, McDermott TR, Copié V et al. 2017. Metabolic response of Agrobacterium tumefaciens 5A to arsenite. Environ. Microbiol. 19:710–21
    [Google Scholar]
  149. 149. 
    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
    [Google Scholar]
  150. 150. 
    Vincent M, Duval R, Hartemann P, Engels-Deutsch M. 2018. Contact killing and antimicrobial properties of copper. J. Appl. Microbiol. 124:1032–46
    [Google Scholar]
  151. 151. 
    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
    [Google Scholar]
  152. 152. 
    Waksman SA. 1947. What is an antibiotic or an antibiotic substance?. Mycologia 39:565–69
    [Google Scholar]
  153. 153. 
    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
    [Google Scholar]
  154. 154. 
    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
    [Google Scholar]
  155. 155. 
    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
    [Google Scholar]
  156. 156. 
    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
    [Google Scholar]
  157. 157. 
    Yan Y, Chen J, Galván 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
    [Google Scholar]
  158. 158. 
    Yang HC, Rosen BP. 2016. New mechanisms of bacterial arsenic resistance. Biomed. J. 39:5–13
    [Google Scholar]
  159. 159. 
    Yang Z, Peng H, Lu X, Liu Q, Huang R et al. 2016. Arsenic metabolites, including N-acetyl-4-hydroxy-m-arsanilic acid, in chicken litter from a roxarsone-feeding study involving 1600 chickens. Environ. Sci. Technol. 50:6737–43
    [Google Scholar]
  160. 160. 
    Yoshinaga M, Cai Y, Rosen BP. 2011. Demethylation of methylarsonic acid by a microbial community. Environ. Microbiol. 13:1205–15
    [Google Scholar]
  161. 161. 
    Yoshinaga M, Rosen BP 2014. A C⋅As lyase for degradation of environmental organoarsenical herbicides and animal husbandry growth promoters. PNAS 111:7701–6
    [Google Scholar]
  162. 162. 
    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
    [Google Scholar]
  163. 163. 
    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
    [Google Scholar]
  164. 164. 
    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
    [Google Scholar]
  165. 165. 
    Zhu YG, Yoshinaga M, Zhao FJ, Rosen BP. 2014. Earth abides arsenic biotransformations. Annu. Rev. Earth Planet. Sci. 42:443–67
    [Google Scholar]
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