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Extracellular electron uptake by autotrophic microbes: physiological, ecological, and evolutionary implications

  • Environmental Microbiology - Mini Review
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

Microbes exchange electrons with their extracellular environment via direct or indirect means. This exchange is bidirectional and supports essential microbial oxidation–reduction processes, such as respiration and photosynthesis. The microbial capacity to use electrons from insoluble electron donors, such as redox-active minerals, poised electrodes, or even other microbial cells is called extracellular electron uptake (EEU). Autotrophs with this capability can thrive in nutrient and soluble electron donor-deficient environments. As primary producers, autotrophic microbes capable of EEU greatly impact microbial ecology and play important roles in matter and energy flow in the biosphere. In this review, we discuss EEU-driven autotrophic metabolisms, their mechanism and physiology, and highlight their ecological, evolutionary, and biotechnological implications.

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References

  1. Agostino V, Rosenbaum MA (2018) Sulfate-reducing electroautotrophs and their applications in bioelectrochemical systems. Front Energy Res 6:55

    Google Scholar 

  2. Albers SV, Meyer BH (2011) The archaeal cell envelope. Nat Rev Microbiol 9:414–426

    CAS  PubMed  Google Scholar 

  3. Amouric A, Brochier-Armanet C, Johnson DB, Bonnefoy V, Hallberg KB (2011) Phylogenetic and genetic variation among Fe(II)-oxidizing Acidithiobacilli supports the view that these comprise multiple species with different ferrous iron oxidation pathways. Microbiology 157:111–122

    CAS  PubMed  Google Scholar 

  4. Appia-Ayme C, Guiliani N, Ratouchniak J, Bonnefoy V (1999) Characterization of an operon encoding two c-type cytochromes, an aa(3)-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 65:4781–4787

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Barco RA, Emerson D, Sylvan JB, Orcutt BN, Jacobson Meyers ME, Ramirez GA, Zhong JD, Edwards KJ (2015) New insight into microbial iron oxidation as revealed by the proteomic profile of an obligate iron-oxidizing chemolithoautotroph. Appl Environ Microbiol 81:5927–5937

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Bartlett KB, Harriss RC (1993) Review and assessment of methane emissions from wetlands. Chemosphere 26:261–320

    CAS  Google Scholar 

  7. Beckwith CR, Edwards MJ, Lawes M, Shi L, Butt JN, Richardson DJ, Clarke TA (2015) Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth. Front Microbiol 6:332

    PubMed  PubMed Central  Google Scholar 

  8. Beese-Vasbender PF, Nayak S, Erbe A, Stratmann M, Mayrhofer KJJ (2015) Electrochemical characterization of direct electron uptake in electrical microbially influenced corrosion of iron by the lithoautotrophic SRB Desulfopila corrodens strain IS4. Electrochim Acta 167:321–329

    CAS  Google Scholar 

  9. Berg IA, Kockelkorn D, Ramos-Vera WH, Say RF, Zarzycki J, Hugler M, Alber BE, Fuchs G (2010) Autotrophic carbon fixation in archaea. Nat Rev Microbiol 8:447–460

    CAS  PubMed  Google Scholar 

  10. Bird LJ, Bonnefoy V, Newman DK (2011) Bioenergetic challenges of microbial iron metabolisms. Trends Microbiol 19:330–340

    CAS  PubMed  Google Scholar 

  11. Bird LJ, Saraiva IH, Park S, Calçada EO, Salgueiro CA, Nitschke W, Louro RO, Newman DK (2014) Nonredundant roles for cytochrome c2 and two high-potential iron-sulfur proteins in the photoferrotroph Rhodopseudomonas palustris TIE-1. J Bacteriol 196:850–858

    PubMed  PubMed Central  Google Scholar 

  12. Boschker HT, Vasquez-Cardenas D, Bolhuis H, Moerdijk-Poortvliet TW, Moodley L (2014) Chemoautotrophic carbon fixation rates and active bacterial communities in intertidal marine sediments. PLoS ONE 9:e101443

    PubMed  PubMed Central  Google Scholar 

  13. Bose A, Gardel EJ, Vidoudez C, Parra EA, Girguis PR (2014) Electron uptake by iron-oxidizing phototrophic bacteria. Nat Commun 5:3391

    CAS  PubMed  Google Scholar 

  14. Brutinel ED, Gralnick JA (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biotechnol 93:41–48

    PubMed  Google Scholar 

  15. Bryce C, Blackwell N, Straub D, Kleindienst S, Kappler A (2019) Draft genome sequence of Chlorobium sp. strain N1, a marine Fe(II)-oxidizing green sulfur bacterium. Microbiol Resour Announc 8:e00080–e119

    PubMed  PubMed Central  Google Scholar 

  16. Brysch K, Schneider C, Fuchs G, Widdel F (1987) Lithoautotrophic growth of sulfate-reducing bacteria, and description of Desulfobacterium autotrophicum gen. nov., sp. nov. Arch Microbiol 148:264–274

    CAS  Google Scholar 

  17. Buckel W, Thauer RK (2018) Flavin-based electron bifurcation, a new mechanism of biological energy coupling. Chem Rev 118:3862–3886

    CAS  PubMed  Google Scholar 

  18. Byrne JM, Klueglein N, Pearce C, Rosso KM, Appel E, Kappler A (2015) Redox cycling of Fe (II) and Fe (III) in magnetite by Fe-metabolizing bacteria. Science 347:1473–1476

    CAS  PubMed  Google Scholar 

  19. Camacho A, Walter XA, Picazo A, Zopfi J (2017) Photoferrotrophy: remains of an ancient photosynthesis in modern environments. Front Microbiol 8:323

    PubMed  PubMed Central  Google Scholar 

  20. Canfield DE, Rosing MT, Bjerrum C (2006) Early anaerobic metabolisms. Philos Trans R Soc Lond B Biol Sci 361:1819–1834

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Canfield DE, Stewart FJ, Thamdrup B, De Brabandere L, Dalsgaard T, Delong EF, Revsbech NP, Ulloa O (2010) A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science 330:1375–1378

    CAS  PubMed  Google Scholar 

  22. Cao X, Huang X, Liang P, Boon N, Fan M, Zhang L, Zhang X (2009) A completely anoxic microbial fuel cell using a photo-biocathode for cathodic carbon dioxide reduction. Energy Environ Sci 2:498–501

    CAS  Google Scholar 

  23. Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G, Brugna M, Giudici-Orticoni MT (2008) A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J Biol Chem 283:25803–25811

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Chan CS, McAllister SM, Garber A, Hallahan BJ, Rozovsky S (2018) Fe oxidation by a fused cytochrome–porin common to diverse Fe-oxidizing bacteria. bioRxiv:228056

  25. Chang R, Bird L, Barr C, Osburn M, Wilbanks E, Nealson K, Rowe A (2018) Thioclava electrotropha sp. nov., a versatile electrode and sulfur-oxidizing bacterium from marine sediments. Int J Syst Evol Microbiol 68:1652–1658

    CAS  PubMed  Google Scholar 

  26. Chen Y, Suzuki I (2004) Effect of uncouplers on endogenous respiration and ferrous iron oxidation in a chemolithoautotrophic bacterium Acidithiobacillus (Thiobacillus) ferrooxidans. FEMS Microbiol Lett 237:139–145

    CAS  PubMed  Google Scholar 

  27. Cheng S, Xing D, Call DF, Logan BE (2009) Direct biological conversion of electrical current into methane by electromethanogenesis. Environ Sci Technol 43:3953–3958

    CAS  PubMed  Google Scholar 

  28. Crichton RR, Pierre JL (2001) Old iron, young copper: from Mars to Venus. Biometals 14:99–112

    CAS  PubMed  Google Scholar 

  29. Croal LR, Jiao Y, Newman DK (2007) The fox operon from Rhodobacter strain SW2 promotes phototrophic Fe(II) oxidation in Rhodobacter capsulatus SB1003. J Bacteriol 189:1774–1782

    CAS  PubMed  Google Scholar 

  30. Crowe SA, Hahn AS, Morgan-Lang C, Thompson KJ, Simister RL, Lliros M, Hirst M, Hallam SJ (2017) Draft genome sequence of the pelagic photoferrotroph Chlorobium phaeoferrooxidans. Genome Announc 5:e01584-16

    PubMed  PubMed Central  Google Scholar 

  31. Brune DC (1995) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria, vol 2. Springer, Dordrecht, pp 847–870

    Google Scholar 

  32. de Bok FA, Plugge CM, Stams AJ (2004) Interspecies electron transfer in methanogenic propionate degrading consortia. Water Res 38:1368–1375

    PubMed  Google Scholar 

  33. de Campos RT, Rosenbaum MA (2014) Microbial electroreduction: screening for new cathodic biocatalysts. ChemElectroChem 1:1916–1922

    Google Scholar 

  34. Deng X, Dohmae N, Nealson KH, Hashimoto K, Okamoto A (2018) Multi-heme cytochromes provide a pathway for survival in energy-limited environments. Sci Adv 4:eaao5682

    PubMed  PubMed Central  Google Scholar 

  35. Deng X, Okamoto A (2018) Electrode potential dependency of single-cell activity identifies the energetics of slow microbial electron uptake process. Front Microbiol 9:2744

    PubMed  PubMed Central  Google Scholar 

  36. Deutzmann JS, Sahin M, Spormann AM (2015) Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. miBo 6:e00496-00415

    Google Scholar 

  37. Dinh HT, Kuever J, Mussmann M, Hassel AW, Stratmann M, Widdel F (2004) Iron corrosion by novel anaerobic microorganisms. Nature 427:829–832

    CAS  PubMed  Google Scholar 

  38. Drake HL, Gossner AS, Daniel SL (2008) Old acetogens, new light. Ann N Y Acad Sci 1125:100–128

    CAS  PubMed  Google Scholar 

  39. Ehrenreich A, Widdel F (1994) Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl Environ Microbiol 60:4517–4526

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Emerson D, Field EK, Chertkov O, Davenport KW, Goodwin L, Munk C, Nolan M, Woyke T (2013) Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics. Front Microbiol 4:254

    PubMed  PubMed Central  Google Scholar 

  41. Emerson D, Moyer C (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63:4784–4792

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Emerson D, Rentz JA, Lilburn TG, Davis RE, Aldrich H, Chan C, Moyer CL (2007) A novel lineage of proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS ONE 2:e667

    PubMed  PubMed Central  Google Scholar 

  43. Enning D, Garrelfs J (2014) Corrosion of iron by sulfate-reducing bacteria: new views of an old problem. Appl Environ Microbiol 80:1226–1236

    PubMed  PubMed Central  Google Scholar 

  44. Esparza M, Cardenas JP, Bowien B, Jedlicki E, Holmes DS (2010) Genes and pathways for CO2 fixation in the obligate, chemolithoautotrophic acidophile, Acidithiobacillus ferrooxidans, carbon fixation in A. ferrooxidans. BMC Microbiol 10:229

    PubMed  PubMed Central  Google Scholar 

  45. Ferguson SJ, Ingledew WJ (2008) Energetic problems faced by micro-organisms growing or surviving on parsimonious energy sources and at acidic pH: I. Acidithiobacillus ferrooxidans as a paradigm. Biochim Biophys Acta 1777:1471–1479

    CAS  PubMed  Google Scholar 

  46. Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism? Appl Environ Microbiol 67:2873–2882

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Garber AI, Nealson KH, Okamoto A, McAllister SM, Chan CS, Barco RA, Merino N (2020) FeGenie: a comprehensive tool for the identification of iron genes and iron gene neighborhoods in genome and metagenome assemblies. Front Microbiol 11:37

    PubMed  PubMed Central  Google Scholar 

  48. Glasser NR, Kern SE, Newman DK (2014) Phenazine redox cycling enhances anaerobic survival in Pseudomonas aeruginosa by facilitating generation of ATP and a proton-motive force. Mol Microbiol 92:399–412

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Gregoire KP, Glaven SM, Hervey J, Lin B, Tender LM (2014) Enrichment of a high-current density denitrifying microbial biocathode. J Electrochem Soc 161:H3049–H3057

    Google Scholar 

  50. Gregory KB, Bond DR, Lovley DR (2004) Graphite electrodes as electron donors for anaerobic respiration. Environ Microbiol 6:596–604

    CAS  PubMed  Google Scholar 

  51. Gupta D, Guzman MS, Bose A (2019) Draft genome sequence of a marine photoferrotrophic bacterium, Rhodovulum robiginosum DSM 12329T. Microbiol Resour Announc 8:e01684–e1718

    PubMed  PubMed Central  Google Scholar 

  52. Gupta D, Sutherland MC, Rengasamy K, Meacham JM, Kranz RG, Bose A (2019) Photoferrotrophs produce a PioAB electron conduit for extracellular electron uptake. mBio 10:e02668-19

    PubMed  PubMed Central  Google Scholar 

  53. Guzman MS, Rengasamy K, Binkley MM, Jones C, Ranaivoarisoa TO, Singh R, Fike DA, Meacham JM, Bose A (2019) Phototrophic extracellular electron uptake is linked to carbon dioxide fixation in the bacterium Rhodopseudomonas palustris. Nat Commun 10:1355

    PubMed  PubMed Central  Google Scholar 

  54. Ha PT, Lindemann SR, Shi L, Dohnalkova AC, Fredrickson JK, Madigan MT, Beyenal H (2017) Syntrophic anaerobic photosynthesis via direct interspecies electron transfer. Nat Commun 8:13924

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Hallbeck L, Stahl F, Pedersen K (1993) Phylogeny and phenotypic characterization of the stalk-forming and iron-oxidizing bacterium Gallionella ferruginea. J Gen Microbiol 139:1531–1535

    CAS  PubMed  Google Scholar 

  56. Han X, Tomaszewski EJ, Sorwat J, Pan Y, Kappler A, Byrne JM (2020) Oxidation of green rust by anoxygenic phototrophic Fe(II)-oxidising bacteria. Geochem Perspect Let 12:52–57

    Google Scholar 

  57. Hawley AK, Brewer HM, Norbeck AD, Pasa-Tolic L, Hallam SJ (2014) Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes. Proc Natl Acad Sci USA 111:11395–11400

    CAS  PubMed  Google Scholar 

  58. He S, Barco RA, Emerson D, Roden EE (2017) Comparative genomic analysis of neutrophilic iron(II) oxidizer genomes for candidate genes in extracellular electron transfer. Front Microbiol 8:1584

    PubMed  PubMed Central  Google Scholar 

  59. He S, Tominski C, Kappler A, Behrens S, Roden EE (2016) Metagenomic analyses of the autotrophic Fe(II)-oxidizing, nitrate-reducing enrichment culture KS. Appl Environ Microbiol 82:2656–2668

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Hedrich S, Schlomann M, Johnson DB (2011) The iron-oxidizing proteobacteria. Microbiology 157:1551–1564

    CAS  PubMed  Google Scholar 

  61. Holmes DE, Rotaru AE, Ueki T, Shrestha PM, Ferry JG, Lovley DR (2018) Electron and proton flux for carbon dioxide reduction in Methanosarcina barkeri during direct interspecies electron transfer. Front Microbiol 9:3109

    PubMed  PubMed Central  Google Scholar 

  62. Holmes DE, Ueki T, Tang HY, Zhou J, Smith JA, Chaput G, Lovley DR (2019) A membrane-bound cytochrome enables Methanosarcina acetivorans to conserve energy from extracellular electron transfer. mBio 10:e00789-19

    PubMed  PubMed Central  Google Scholar 

  63. Huang L, Liu X, Tang J, Yu L, Zhou S (2019) Electrochemical evidence for direct interspecies electron transfer between Geobacter sulfurreducens and Prosthecochloris aestuarii. Bioelectrochemistry 127:21–25

    CAS  PubMed  Google Scholar 

  64. Igarashi K, Kato S (2017) Extracellular electron transfer in acetogenic bacteria and its application for conversion of carbon dioxide into organic compounds. Appl Microbiol Biotechnol 101:6301–6307

    CAS  PubMed  Google Scholar 

  65. Ingledew WJ (1982) Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta 683:89–117

    CAS  PubMed  Google Scholar 

  66. Ishii S, Kosaka T, Hori K, Hotta Y, Watanabe K (2005) Coaggregation facilitates interspecies hydrogen transfer between Pelotomaculum thermopropionicum and Methanothermobacter thermautotrophicus. Appl Environ Microbiol 71:7838–7845

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Ishii S, Kosaka T, Hotta Y, Watanabe K (2006) Simulating the contribution of coaggregation to interspecies hydrogen fluxes in syntrophic methanogenic consortia. Appl Environ Microbiol 72:5093–5096

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Ishii T, Kawaichi S, Nakagawa H, Hashimoto K, Nakamura R (2015) From chemolithoautotrophs to electrolithoautotrophs: CO2 fixation by Fe(II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources. Front Microbiol 6:994

    PubMed  PubMed Central  Google Scholar 

  69. Jansen K, Thauer RK, Widdel F, Fuchs G (1984) Carbon assimilation pathways in sulfate reducing bacteria. Formate, carbon dioxide, carbon monoxide, and acetate assimilation by Desulfovibrio baarsii. Arch Microbiol 138:257–262

    CAS  Google Scholar 

  70. Jeans C, Singer SW, Chan CS, Verberkmoes NC, Shah M, Hettich RL, Banfield JF, Thelen MP (2008) Cytochrome 572 is a conspicuous membrane protein with iron oxidation activity purified directly from a natural acidophilic microbial community. ISME J 2:542–550

    CAS  PubMed  Google Scholar 

  71. Jiao Y, Newman DK (2007) The pio operon is essential for phototrophic Fe (II) oxidation in Rhodopseudomonas palustris TIE-1. J Bacteriol 189:1765–1773

    CAS  PubMed  Google Scholar 

  72. Jorgensen CJ, Jacobsen OS, Elberling B, Aamand J (2009) Microbial oxidation of pyrite coupled to nitrate reduction in anoxic groundwater sediment. Environ Sci Technol 43:4851–4857

    PubMed  Google Scholar 

  73. Kappler A, Newman DK (2004) Formation of Fe (III)-minerals by Fe (II)-oxidizing photoautotrophic bacteria. Geochim Cosmochim 68:1217–1226

    CAS  Google Scholar 

  74. Karbelkar AA, Rowe AR, El-Naggar MY (2019) An electrochemical investigation of interfacial electron uptake by the sulfur oxidizing bacterium Thioclava electrotropha ElOx9. Electrochim Acta 324:134838

    CAS  Google Scholar 

  75. Kato S, Ohkuma M, Powell DH, Krepski ST, Oshima K, Hattori M, Shapiro N, Woyke T, Chan CS (2015) Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria. Front Microbiol 6:1265

    PubMed  PubMed Central  Google Scholar 

  76. Kato S, Yumoto I, Kamagata Y (2015) Isolation of acetogenic bacteria that induce biocorrosion by utilizing metallic iron as the sole electron donor. Appl Environ Microbiol 81:67–73

    PubMed  Google Scholar 

  77. Kletzin A, Heimerl T, Flechsler J, van Niftrik L, Rachel R, Klingl A (2015) Cytochromes c in Archaea: distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis. Front Microbiol 6:439

    PubMed  PubMed Central  Google Scholar 

  78. Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334

    CAS  PubMed  Google Scholar 

  79. Konhauser KO, Hamade T, Raiswell R, Morris RC, Ferris FG, Southam G, Canfield DE (2002) Could bacteria have formed the Precambrian banded iron formations? Geology 30:1079–1082

    CAS  Google Scholar 

  80. Konhauser KO, Kappler A, Roden EE (2011) Iron in microbial metabolisms. Elements 7:89–93

    CAS  Google Scholar 

  81. Kotloski NJ, Gralnick JA (2013) Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis. mBio 4:e00553-12

    PubMed  PubMed Central  Google Scholar 

  82. Lam BR, Barr CR, Rowe AR, Nealson KH (2019) Differences in applied redox potential on cathodes enrich for diverse electrochemically active microbial isolates from a marine sediment. Front Microbiol 10:1979

    PubMed  PubMed Central  Google Scholar 

  83. Lam BR, Rowe AR, Nealson KH (2018) Variation in electrode redox potential selects for different microorganisms under cathodic current flow from electrodes in marine sediments. Environ Microbiol 20:2270–2287

    CAS  PubMed  Google Scholar 

  84. Lemaire ON, Jespersen M, Wagner T (2020) CO2-fixation strategies in energy extremophiles: what can we learn from acetogens? Front Microbiol 11:486

    PubMed  PubMed Central  Google Scholar 

  85. Liu J, Wang Z, Belchik SM, Edwards MJ, Liu C, Kennedy DW, Merkley ED, Lipton MS, Butt JN, Richardson DJ (2012) Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe (II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front Microbiol 3:37

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Llorens-Mares T, Yooseph S, Goll J, Hoffman J, Vila-Costa M, Borrego CM, Dupont CL, Casamayor EO (2015) Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics. ISME J 9:1648–1661

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Logan BE (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381

    CAS  PubMed  Google Scholar 

  88. Lovley DR (2008) Extracellular electron transfer: wires, capacitors, iron lungs, and more. Geobiology 6:225–231

    CAS  PubMed  Google Scholar 

  89. Lovley DR (2017) Syntrophy goes electric: direct interspecies electron transfer. Annu Rev Microbiol 71:643–664

    CAS  PubMed  Google Scholar 

  90. Lovley DR, Nevin KP (2013) Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr Opin Biotechnol 24:385–390

    CAS  PubMed  Google Scholar 

  91. Luther GW 3rd, Findlay AJ, Macdonald DJ, Owings SM, Hanson TE, Beinart RA, Girguis PR (2011) Thermodynamics and kinetics of sulfide oxidation by oxygen: a look at inorganically controlled reactions and biologically mediated processes in the environment. Front Microbiol 2:62

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Marshall CW, Ross DE, Handley KM, Weisenhorn PB, Edirisinghe JN, Henry CS, Gilbert JA, May HD, Norman RS (2017) Metabolic reconstruction and modeling microbial electrosynthesis. Sci Rep 7:8391

    PubMed  PubMed Central  Google Scholar 

  93. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA 105:3968–3973

    CAS  PubMed  Google Scholar 

  94. Martin WF, Thauer RK (2017) Energy in ancient metabolism. Cell 168:953–955

    CAS  PubMed  Google Scholar 

  95. Mattes TE, Nunn BL, Marshall KT, Proskurowski G, Kelley DS, Kawka OE, Goodlett DR, Hansell DA, Morris RM (2013) Sulfur oxidizers dominate carbon fixation at a biogeochemical hot spot in the dark ocean. ISME J 7:2349–2360

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Matthews E, Fung I (1987) Methane emission from natural wetlands: Global distribution, area, and environmental characteristics of sources. Glob Biogeochem Cycles 1:61–86

    CAS  Google Scholar 

  97. McAllister SM, Moore RM, Gartman A, Luther GW, Emerson D, Chan CS (2019) The Fe(II)-oxidizing Zetaproteobacteria: historical, ecological and genomic perspectives. FEMS Microbiol Ecol 95:fiz015

    CAS  PubMed  PubMed Central  Google Scholar 

  98. McAllister SM, Polson SW, Butterfield DA, Glazer BT, Sylvan JB, Chan CS (2020) Validating the Cyc2 neutrophilic iron oxidation pathway using meta-omics of zetaproteobacteria iron mats at marine hydrothermal vents. mSystems 5:e00553-19

    PubMed  PubMed Central  Google Scholar 

  99. McGlynn SE (2017) Energy metabolism during anaerobic methane oxidation in ANME Archaea. Microbes Environ 32:5–13

    PubMed  PubMed Central  Google Scholar 

  100. McGlynn SE, Chadwick GL, Kempes CP, Orphan VJ (2015) Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526:531–535

    CAS  PubMed  Google Scholar 

  101. Meyer KM, Kump LR (2008) Oceanic Euxinia in earth history: causes and consequences. Annu Rev Earth Planet Sci 36:251–288

    CAS  Google Scholar 

  102. Meyerdierks A, Kube M, Kostadinov I, Teeling H, Glockner FO, Reinhardt R, Amann R (2010) Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group. Environ Microbiol 12:422–439

    CAS  PubMed  Google Scholar 

  103. Mishra D, Rhee YH (2014) Microbial leaching of metals from solid industrial wastes. J Microbiol 52:1–7

    CAS  PubMed  Google Scholar 

  104. Mishra S, Pirbadian S, Mondal AK, El-Naggar MY, Naaman R (2019) Spin-dependent electron transport through bacterial cell surface multiheme electron conduits. J Am Chem Soc 141:19198–19202

    CAS  PubMed  Google Scholar 

  105. Nauhaus K, Treude T, Boetius A, Kruger M (2005) Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities. Environ Microbiol 7:98–106

    CAS  PubMed  Google Scholar 

  106. Nevin KP, Hensley SA, Franks AE, Summers ZM, Ou J, Woodard TL, Snoeyenbos-West OL, Lovley DR (2011) Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microbiol 77:2882–2886

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Nevin KP, Woodard TL, Franks AE, Summers ZM, Lovley DR (2010) Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. mBio 1:e00103-10

    PubMed  PubMed Central  Google Scholar 

  108. Pereira L, Saraiva IH, Oliveira ASF, Soares CM, Louro RO, Frazao C (2017) Molecular structure of FoxE, the putative iron oxidase of Rhodobacter ferrooxidans SW2. Biochim Biophys Acta Bioenerg 1858:847–853

    CAS  PubMed  Google Scholar 

  109. Peters JW, Beratan DN, Bothner B, Dyer RB, Harwood CS, Heiden ZM, Hille R, Jones AK, King PW, Lu Y, Lubner CE, Minteer SD, Mulder DW, Raugei S, Schut GJ, Seefeldt LC, Tokmina-Lukaszewska M, Zadvornyy OA, Zhang P, Adams MW (2018) A new era for electron bifurcation. Curr Opin Chem Biol 47:32–38

    CAS  PubMed  Google Scholar 

  110. Philips J (2019) Extracellular electron uptake by acetogenic bacteria: does H2 consumption favor the H2 evolution reaction on a cathode or metallic iron? Front Microbiol 10:2997

    PubMed  Google Scholar 

  111. Philips J, Monballyu E, Georg S, De Paepe K, Prevoteau A, Rabaey K, Arends JBA (2019) An Acetobacterium strain isolated with metallic iron as electron donor enhances iron corrosion by a similar mechanism as Sporomusa sphaeroides. FEMS Microbiol Ecol 95:fiy222

    CAS  Google Scholar 

  112. Pierson B, Parenteau M, Griffin B (1999) Phototrophs in high-iron-concentration microbial mats: physiological ecology of phototrophs in an iron-depositing hot spring. Appl Environ Microbiol 65:5474–5483

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Prevoteau A, Carvajal-Arroyo JM, Ganigue R, Rabaey K (2020) Microbial electrosynthesis from CO2: forever a promise? Curr Opin Biotechnol 62:48–57

    CAS  PubMed  Google Scholar 

  114. Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes DS, Bonnefoy V (2009) Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genom 10:394

    Google Scholar 

  115. Rabaey K, Rodriguez J, Blackall LL, Keller J, Gross P, Batstone D, Verstraete W, Nealson KH (2007) Microbial ecology meets electrochemistry: electricity-driven and driving communities. ISME J 1:9–18

    CAS  PubMed  Google Scholar 

  116. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis—revisiting the electrical route for microbial production. Nat Rev Microbiol 8:706–716

    CAS  PubMed  Google Scholar 

  117. Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood–Ljungdahl pathway of CO(2) fixation. Biochim Biophys Acta 1784:1873–1898

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Ranaivoarisoa TO, Singh R, Rengasamy K, Guzman MS, Bose A (2019) Towards sustainable bioplastic production using the photoautotrophic bacterium Rhodopseudomonas palustris TIE-1. J Ind Microbiol Biotechnol 46:1401–1417

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Reeburgh WS (2007) Oceanic methane biogeochemistry. Chem Rev 107:486–513

    CAS  PubMed  Google Scholar 

  120. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101

    CAS  PubMed  Google Scholar 

  121. Ross DE, Flynn JM, Baron DB, Gralnick JA, Bond DR (2011) Towards electrosynthesis in Shewanella: energetics of reversing the mtr pathway for reductive metabolism. PLoS ONE 6:e16649

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Rotaru AE, Shrestha PM, Liu F, Markovaite B, Chen S, Nevin KP, Lovley DR (2014) Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol 80:4599–4605

    PubMed  PubMed Central  Google Scholar 

  123. Rowe AR, Chellamuthu P, Lam B, Okamoto A, Nealson KH (2014) Marine sediments microbes capable of electrode oxidation as a surrogate for lithotrophic insoluble substrate metabolism. Front Microbiol 5:784

    PubMed  Google Scholar 

  124. Rowe AR, Xu S, Gardel E, Bose A, Girguis P, Amend JP, El-Naggar MY (2019) Methane-linked mechanisms of electron uptake from cathodes by Methanosarcina barkeri. mBio 10:e02448-18

    PubMed  PubMed Central  Google Scholar 

  125. Schauder R, Widdel F, Fuchs G (1987) Carbon assimilation pathways in sulfate-reducing bacteria II. Enzymes of a reductive citric acid cycle in the autotrophic Desulfobacter hydrogenophilus. Arch Microbiol 148:218–225

    CAS  Google Scholar 

  126. Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ (2016) Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351:703–707

    CAS  PubMed  Google Scholar 

  127. Schuchmann K, Muller V (2013) Direct and reversible hydrogenation of CO2 to formate by a bacterial carbon dioxide reductase. Science 342:1382–1385

    CAS  PubMed  Google Scholar 

  128. Schuchmann K, Muller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12:809–821

    CAS  PubMed  Google Scholar 

  129. Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, Yu HQ, Fredrickson JK (2016) Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 14:651–662

    CAS  PubMed  Google Scholar 

  130. Shi L, Rosso KM, Zachara JM, Fredrickson JK (2012) Mtr extracellular electron-transfer pathways in Fe(III)-reducing or Fe(II)-oxidizing bacteria: a genomic perspective. Biochem Soc Trans 40:1261–1267

    CAS  PubMed  Google Scholar 

  131. Shi L, Squier TC, Zachara JM, Fredrickson JK (2007) Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65:12–20

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Shrestha PM, Rotaru AE (2014) Plugging in or going wireless: strategies for interspecies electron transfer. Front Microbiol 5:237

    PubMed  PubMed Central  Google Scholar 

  133. Shrestha PM, Rotaru AE, Summers ZM, Shrestha M, Liu F, Lovley DR (2013) Transcriptomic and genetic analysis of direct interspecies electron transfer. Appl Environ Microbiol 79:2397–2404

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Sievert SM, Hugler M, Taylor CD, Wirsen CO (2008) Sulfur oxidation at deep-sea hydrothermal vents. In: Dahl CFCG (ed) Microbial sulfur metabolism. Springer, Berlin, pp 238–258

    Google Scholar 

  135. Skennerton CT, Chourey K, Iyer R, Hettich RL, Tyson GW, Orphan VJ (2017) Methane-fueled syntrophy through extracellular electron transfer: uncovering the genomic traits conserved within diverse bacterial partners of anaerobic methanotrophic Archaea. mBio 8:e00530-17

    PubMed  PubMed Central  Google Scholar 

  136. Song J, Kim Y, Lim M, Lee H, Lee JI, Shin W (2011) Microbes as electrochemical CO2 conversion catalysts. Chemsuschem 4:587–590

    CAS  PubMed  Google Scholar 

  137. Sorokin DY, Tourova TP, Spiridonova EM, Rainey FA, Muyzer G (2005) Thioclava pacifica gen. nov., sp. nov., a novel facultatively autotrophic, marine, sulfur-oxidizing bacterium from a near-shore sulfidic hydrothermal area. Int J Syst Evol Microbiol 55:1069–1075

    CAS  PubMed  Google Scholar 

  138. Strycharz-Glaven SM, Glaven RH, Wang Z, Zhou J, Vora GJ, Tender LM (2013) Electrochemical investigation of a microbial solar cell reveals a nonphotosynthetic biocathode catalyst. Appl Environ Microbiol 79:3933–3942

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR (2010) Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330:1413–1415

    CAS  PubMed  Google Scholar 

  140. Summers ZM, Gralnick JA, Bond DR (2013) Cultivation of an obligate Fe(II)-oxidizing lithoautotrophic bacterium using electrodes. mBio 4:e00420-12

    PubMed  PubMed Central  Google Scholar 

  141. Tremblay P-LF, Zhang T (2019) Accelerated H2 evolution during microbial electrosynthesis with Sporomusa ovata. Catalysts 9:166

    Google Scholar 

  142. Tremblay PL, Angenent LT, Zhang T (2017) Extracellular electron uptake: among autotrophs and mediated by surfaces. Trends Biotechnol 35:360–371

    CAS  PubMed  Google Scholar 

  143. Tsurumaru H, Ito N, Mori K, Wakai S, Uchiyama T, Iino T, Hosoyama A, Ataku H, Nishijima K, Mise M, Shimizu A, Harada T, Horikawa H, Ichikawa N, Sekigawa T, Jinno K, Tanikawa S, Yamazaki J, Sasaki K, Yamazaki S, Fujita N, Harayama S (2018) An extracellular [NiFe] hydrogenase mediating iron corrosion is encoded in a genetically unstable genomic island in Methanococcus maripaludis. Sci Rep 8:15149

    PubMed  PubMed Central  Google Scholar 

  144. Valdes J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake R 2nd, Eisen JA, Holmes DS (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genom 9:597

    Google Scholar 

  145. Van Driessche G, Vandenberghe I, Devreese B, Samyn B, Meyer TE, Leigh R, Cusanovich MA, Bartsch RG, Fischer U, Van Beeumen JJ (2003) Amino acid sequences and distribution of high-potential iron-sulfur proteins that donate electrons to the photosynthetic reaction center in phototropic proteobacteria. J Mol Evol 57:181–199

    PubMed  Google Scholar 

  146. Villano M, Aulenta F, Ciucci C, Ferri T, Giuliano A, Majone M (2010) Bioelectrochemical reduction of CO2 to CH4 via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture. Bioresour Technol 101:3085–3090

    CAS  PubMed  Google Scholar 

  147. Wacey D, Kilburn MR, Saunders M, Cliff J, Brasier MD (2011) Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia. Nat Geosci 4:698–702

    CAS  Google Scholar 

  148. Wang FP, Zhang Y, Chen Y, He Y, Qi J, Hinrichs KU, Zhang XX, Xiao X, Boon N (2014) Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways. ISME J 8:1069–1078

    CAS  PubMed  Google Scholar 

  149. Wang Y, Kern SE, Newman DK (2010) Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192:365–369

    CAS  PubMed  Google Scholar 

  150. Wegener G, Krukenberg V, Riedel D, Tegetmeyer HE, Boetius A (2015) Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526:587–590

    CAS  PubMed  Google Scholar 

  151. Wegener G, Krukenberg V, Ruff SE, Kellermann MY, Knittel K (2016) Metabolic capabilities of microorganisms involved in and associated with the anaerobic oxidation of methane. Front Microbiol 7:46

    PubMed  PubMed Central  Google Scholar 

  152. Widdel F, Schnell S, Heising S, Ehrenreich A, Assmus B, Schink B (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362:834–836

    CAS  Google Scholar 

  153. Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730

    CAS  PubMed  Google Scholar 

  154. Yamamoto M, Takai K (2011) Sulfur metabolisms in epsilon- and gamma-proteobacteria in deep-sea hydrothermal fields. Front Microbiol 2:192

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Yarzabal A, Appia-Ayme C, Ratouchniak J, Bonnefoy V (2004) Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology 150:2113–2123

    CAS  PubMed  Google Scholar 

  156. Yarzabal A, Brasseur G, Ratouchniak J, Lund K, Lemesle-Meunier D, DeMoss JA, Bonnefoy V (2002) The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol 184:313–317

    CAS  PubMed  PubMed Central  Google Scholar 

  157. Yee MO, Rotaru AE (2020) Extracellular electron uptake in Methanosarcinales is independent of multiheme c-type cytochromes. Sci Rep 10:372

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Yee MO, Snoeyenbos-West OL, Thamdrup B, Ottosen LDM, Rotaru A-E (2019) Extracellular electron uptake by two Methanosarcina species. Front Energy Res 7:458091

    Google Scholar 

  159. Zaybak Z, Logan BE, Pisciotta JM (2018) Electrotrophic activity and electrosynthetic acetate production by Desulfobacterium autotrophicum HRM2. Bioelectrochemistry 123:150–155

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to acknowledge financial support from the U.S. Department of Energy to A.B. (Grant Number DESC0014613), the David and Lucile Packard Foundation to A.B. (Grant Number 201563111), the Gordon and Betty Moore Foundation to A.B., the U.S. Department of Defense, Army Research Office to A.B. (Grant Number W911NF-18-1-0037) and the National Science Foundation to A.B.(Grant Number 2021822). M.G. performed this work under the auspices of the U.S. Department of Energy by Lawrence Livermore National Laboratory under Contract DEAC5207NA27344 (LLNL-JRNL-812309) to A.B. and M.G.

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  1. Dinesh Gupta and Michael S. Guzman contributed equally to this work.

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  1. Department of Biology, Washington University in St. Louis, One Brookings Drive, St. Louis, MO, 63130, USA

    Dinesh Gupta & Arpita Bose

  2. Biosciences and Biotechnology Division, Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, USA

    Michael S. Guzman

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DG, MSG, and AB performed the necessary literature search. DG, MSG, and AB wrote the manuscript and did critical reading to shape the manuscript. DG and MSG contributed equally to this work. All authors reviewed and contributed to the final version of the manuscript.

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Correspondence to Arpita Bose.

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Gupta, D., Guzman, M.S. & Bose, A. Extracellular electron uptake by autotrophic microbes: physiological, ecological, and evolutionary implications. J Ind Microbiol Biotechnol 47, 863–876 (2020). https://doi.org/10.1007/s10295-020-02309-0

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