1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Microbiology
  4. Volume 71, 2017
  5. Article

Annual Review of Microbiology

Volume 71, 2017

Syntrophy Goes Electric: Direct Interspecies Electron Transfer

Abstract

Direct interspecies electron transfer (DIET) has biogeochemical significance, and practical applications that rely on DIET or DIET-based aspects of microbial physiology are growing. Mechanisms for DIET have primarily been studied in defined cocultures in which species are one of the DIET partners. Electrically conductive pili (e-pili) can be an important electrical conduit for DIET. However, there may be instances in which electrical contacts are made between electron transport proteins associated with the outer membranes of the partners. Alternatively, DIET partners can plug into conductive carbon materials, such as granular activated carbon, carbon cloth, and biochar, for long-range electron exchange without the need for e-pili. Magnetite promotes DIET, possibly by acting as a substitute for outer-surface -type cytochromes. DIET is the primary mode of interspecies electron exchange in some anaerobic digesters converting wastes to methane. Promoting DIET with conductive materials shows promise for stabilizing and accelerating methane production in digesters, permitting higher organic loading rates. Various lines of evidence suggest that DIET is important in terrestrial wetlands, which are an important source of atmospheric methane. DIET may also have a role in anaerobic methane oxidation coupled to sulfate reduction, an important control on methane releases. The finding that DIET can serve as the source of electrons for anaerobic photosynthesis further broadens its potential environmental significance. Microorganisms capable of DIET are good catalysts for several bioelectrochemical technologies and e-pili are a promising renewable source of electronic materials. The study of DIET is in its early stages, and additional investigation is required to better understand the diversity of microorganisms that are capable of DIET, the importance of DIET to carbon and electron flow in anaerobic environments, and the biochemistry and physiology of DIET.

Keyword(s): anaerobic digestion, cytochrome, e-pili, Geobacter, methane oxidation, methane production, Methanosarcina, Methanothrix, Prosthecochloris
Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-030117-020420
2017-09-08
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/71/1/annurev-micro-030117-020420.html?itemId=/content/journals/10.1146/annurev-micro-030117-020420&mimeType=html&fmt=ahah

Literature Cited

  1. Adhikari R. 1.  2016. Study of charge transport mechanism in microbial nanowires PhD Thesis Univ. Mass. Amherst:
  2. Adhikari RY, Malvankar NS, Tuominen MT, Lovley DR. 2.  2016. Conductivity of individual Geobacter pili. RSC Adv 6:8354–57 [Google Scholar]
  3. Altamurea L, Horvath C, Rengaraj S, Rongier A, Elouarzaki K. 3.  et al. 2016. A synthetic redox biofilm made from metalloprotein–prion domain chimera nanowires. Nat. Chem. 9:157–63 [Google Scholar]
  4. Baek G, Kim J, Cho K, Bae H, Lee C. 4.  2015. The biostimulation of anaerobic digestion with (semi)conductive ferric oxides: their potential for enhanced biomethanation. Appl. Microbiol. Biotechnol. 99:10355–66 [Google Scholar]
  5. Baek G, Kim J, Lee C. 5.  2016. A long-term study on the effect of magnetite supplementation in continuous anaerobic digestion of dairy effluent—enhancement in process performance and stability. Bioresour. Technol. 222:344–54 [Google Scholar]
  6. Baracharya S, Sharma M, Mohanakrishna G, Benneton XD, Strik DPBTB. 6.  et al. 2016. An overview on emerging bioelectrochemical systems (BESs): technology for sustainable electricity, waste remediation, resource recovery, chemical production and beyond. Renew. Energy 98:153–70 [Google Scholar]
  7. Benomar S, Ranava D, Cardenas ML, Trably E, Rafrafi Y. 7.  et al. 2015. Nutritional stress induces exchange of cell material and energetic coupling between bacterial species. Nat. Commun. 6:6283 [Google Scholar]
  8. Bond DR, Holmes DE, Tender LM, Lovley DR. 8.  2002. Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–85 [Google Scholar]
  9. Bond DR, Lovley DR. 9.  2003. Electricity production by Geobacter sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 69:1548–55 [Google Scholar]
  10. Bose A, Gardel EJ, Vidoudez C, Parra EA, Girguis PR. 10.  2014. Electron uptake by iron-oxidizing phototrophic bacteria. Nat. Commun. 5:3391 [Google Scholar]
  11. Bryant MP, Wolin EA, Wolin MJ, Wolfe RS. 11.  1967. Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch. Microbiol. 59:20–31 [Google Scholar]
  12. Cao X, Huang X, Liang P, Boon N, Fan M. 12.  et al. 2009. A completely anoxic microbial fuel cell using a photo-biocathode for cathodic carbon dioxide reduction. Energy Environ. Sci. 2:498–501 [Google Scholar]
  13. Castro L, Vera M, Muñoz JA, Blázquez ML, González F. 13.  et al. 2013. Conductive filaments produced by Aeromonas hydrophila. Adv. Mater. Res. 825:210–13 [Google Scholar]
  14. Chen S, Rotaru A-E, Liu F, Philips J, Woodard TL. 14.  et al. 2014. Carbon cloth stimulates direct interspecies electron transfer in syntrophic co-cultures. Bioresour. Technol. 173:82–86 [Google Scholar]
  15. Chen S, Rotaru A-E, Shrestha PM, Malvankar NS, Liu F. 15.  et al. 2014. Promoting interspecies electron transfer with biochar. Sci. Rep. 4:5019 [Google Scholar]
  16. Cheng Q, Call D. 16.  2016. Hardwiring microbes via direct interspecies electron transfer: mechanisms and applications. Environ. Sci. Process. Impacts 18:968–80This study provides an integrated analysis of DIET studies and practical applications. [Google Scholar]
  17. Creasey RCG, Shingaya Y, Nakayama T. 17.  2015. Improved electrical conductance through self-assembly of bioinspired peptides into nanoscale fibers. Mater. Chem. Phys. 158:52–59 [Google Scholar]
  18. Dang Y, Holmes DE, Zhoa Z, Woodard TL, Zhang Y. 18.  et al. 2016. Enhancing anaerobic digestion of complex organic waste with carbon-based conductive materials. Bioresour. Technol. 220:516–22 [Google Scholar]
  19. De Vrieze J, Hennebel T, Boon N, Verstraete W. 19.  2012. Methanosarcina: the rediscovered methanogen for heavy duty biomethanation. Bioresour. Technol. 112:1–9 [Google Scholar]
  20. Doyle LE, Marsili E. 20.  2015. Methods for enrichment of novel electrochemically-active microorganisms. Bioresour. Technol. 195:273–82 [Google Scholar]
  21. Eaktasang N, Kang CS, Lim H, Kwean OS, Cho S. 21.  et al. 2016. Production of electrically-conductive nanoscale filaments by sulfate-reducing bacteria in the microbial fuel cell. Bioresour. Technol. 201:61–67 [Google Scholar]
  22. Esteve-Nunez A, Sosnik J, Visconti P, Lovley DR. 22.  2008. Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens. Environ. Microbiol 10:497–505 [Google Scholar]
  23. Ettwig KF, Zhu B, Speth D, Keltjens JT, Jetten MSM, Kartal B. 23.  2016. Archaea catalyze iron-dependent anaerobic oxidation of methane. PNAS 113:12792–96 [Google Scholar]
  24. Gregory KB, Bond DR, Lovley DR. 24.  2004. Graphite electrodes as electron donors for anaerobic respiration. Environ. Microbiol. 6:596–604 [Google Scholar]
  25. Guterman T, Kornreich M, Stern A, Adler-Abramovich L, Proath D. 25.  et al. 2016. Formation of bacterial pilus-like nanofibres by designed minimalistic self-assembling peptides. Nat. Commun. 7:13482 [Google Scholar]
  26. Ha PT, Lindemann SR, Shi L, Dohnalkova AC, Fredrickson JK. 26.  et al. 2017. Syntrophic anaerobic photosynthesis via direct interspecies electron transfer. Nat. Commun. 7:13924This study presents the first demonstration of a phototroph participating in DIET. [Google Scholar]
  27. Holmes DE, Dang Y, Walker DJF, Lovley DR. 27.  2016. The electrically conductive pili of Geobacter species are a recently evolved feature for extracellular electron transfer. Microb. Genom. 2:e000072 [Google Scholar]
  28. Holmes DE, Shrestha PM, Walker DJF, Dang Y, Nevin KP. 28.  et al. 2017. Metatranscriptomic evidence for direct interspecies electron transfer between Geobacter and Methanothrix species in rice paddy soils. Appl. Environ. Microbiol 83:e00223–17 [Google Scholar]
  29. Hori T, Noll M, Igarashi Y, Friedrich MW, Conrad R. 29.  2007. Identification of acetate-assimilating microorganisms under methanogenic conditions in anoxic rice field soil by comparative stable isotope probing of RNA. Appl. Environ. Microbiol. 73:101–9 [Google Scholar]
  30. Inoue K, Leang C, Franks AE, Woodard TL, Nevin KP, Lovley DR. 30.  2010. Specific localization of the c-type cytochrome OmcZ at the anode surface in current-producing biofilms of Geobacter sulfurreducens. Environ. Microbiol. Rep. 3:211–17 [Google Scholar]
  31. Inoue K, Qian X, Morgado L, Kim B-C, Mester T. 31.  et al. 2010. Purification and characterization of OmcZ, an outer-surface, octaheme, c-type cytochrome essential for optimal current production by Geobacter sulfurreducens. Appl. Environ. Microbiol. 76:3999–4007 [Google Scholar]
  32. Jing Y, Wan J, Angelidaki I, Zhang S, Luo G. 32.  2017. TRAQ quantitative proteomic analysis reveals the pathways for methanation of propionate facilitated by magnetite. Water Res 108:212–21 [Google Scholar]
  33. Kaden J, Galushko AS, Schink B. 33.  2002. Cysteine-mediated electron transfer in syntrophic acetate oxidation by cocultures of Geobactersulfurreducens and Wolinella succinogenes. Arch. Microbiol. 178:53–58 [Google Scholar]
  34. Kalathil S, Pant D. 34.  2016. Nanotechnology to rescue bacterial bidirectional extracellular electron transfer in bioelectrochemical systems. RSC Adv 6:30582–97 [Google Scholar]
  35. Kato S, Hashimoto K, Wantanabe K. 35.  2012. Microbial interspecies electron transfer via electric currents through conductive minerals. PNAS 109:10042–46 [Google Scholar]
  36. Kato S, Hashimoto K, Watanabe K. 36.  2012. Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ. Microbiol. 14:1646–54The first suggestion that magnetite might promote DIET to methanogens is found in this study. [Google Scholar]
  37. Kim Y, Liesack W. 37.  2015. Differential assemblage of functional units in paddy soil microbiomes. PLOS ONE 10:e0122221 [Google Scholar]
  38. Kirkegaard RH, Mcilroy SJ, Kristensen JM, Nierychlo M, Karst SM. 38.  et al. 2017. Identifying the abundant and active microorganisms common to full-scale anaerobic digesters. bioRxiv 104620 https://doi.org/10.1101/104620 [Crossref]
  39. Koch C, Harnisch F. 39.  2016. Is there a specific ecological niche for electroactive microorganisms?. ChemElectroChem 3:1282–95This work represents a comprehensive compilation of microorganisms known to be capable of extracellular electron exchange. [Google Scholar]
  40. Kohler PRA, Metcalf MW. 40.  2012. Genetic manipulation of Methanosarcina spp. Front. Microbiol. 3:259 [Google Scholar]
  41. Krukenberg V, Harding K, Richter M, Glockner FO, Gruber-Vodicka HR. 41.  et al. 2016. Candidatus Desulfofervidus auxilii, a hydrogenotrophic sulfate-reducing bacterium involved in the thermophilic anaerobic oxidation of methane. Environ. Microbiol. 18:3073–91 [Google Scholar]
  42. Larson LL, Liu H. 42.  2014. Establishing a core microbiome in acetate-fed microbial fuel cells. App. Microbiol. Biotechnol. 98:4187 [Google Scholar]
  43. Laso-Pérez R, Wegener G, Knittel K, Widdel F, Harding KJ. 43.  et al. 2016. Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature 539:396–401 [Google Scholar]
  44. Leang C, Coppi MV, Lovley DR. 44.  2003. OmcB, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol 185:2096–103 [Google Scholar]
  45. Leang C, Qian X, Mester T, Lovley DR. 45.  2010. Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl. Environ. Microbiol 76:4080–84 [Google Scholar]
  46. Leang C, Malvankar NS, Franks AE, Nevin KP, Lovley DR. 46.  2013. Engineering Geobacter sulfurreducens to produce a highly cohesive conductive matrix with enhanced capacity for current production. Energy Environ. Sci. 6:1901–8 [Google Scholar]
  47. Lee H-S, Dhar BR, An J, Rittmann BE, Ryu H. 47.  et al. 2016. The roles of biofilm conductivity and donor substrate kinetics in a mixed-culture biofilm anode. Environ. Sci. Technol. 50:12799–807 [Google Scholar]
  48. Lee J-Y, Lee S-H, Park H-D. 48.  2016. Enrichment of specific electro-active microorganisms and enhancement of methane production by adding granular activated carbon in anaerobic reactors. Bioresour. Technol. 205:205–12 [Google Scholar]
  49. Lei Y, Sun D, Dang Y, Chen H, Zhao Z. 49.  et al. 2016. Stimulation of methanogenesis in anaerobic digesters treating leachate from a municipal solid waste incineration plant with carbon cloth. Bioresour. Technol. 222:270–76 [Google Scholar]
  50. Li H, Chang J, Liu P, Fu L, Ding D, Lu Y. 50.  2015. Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments. Environ. Microbiol. 17:1533–47 [Google Scholar]
  51. Li L-L, Tong Z-H, Fang C-Y, Chu J, Yu H-Q. 51.  2015. Response of anaerobic granular sludge to single-wall carbon nanotube exposure. Water Res 70:1–8 [Google Scholar]
  52. Li Y, Li H. 52.  2014. Type IV pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. J. Basic Microbiol. 54:226–31 [Google Scholar]
  53. Liu F, Rotaru A-E, Shrestha PM, Malvankar NS, Nevin KP, Lovley DR. 53.  2012. Promoting direct interspecies electron transfer with activated carbon. Energy Environ. Sci. 5:8982–89This study was first to demonstrate that conductive materials promote long-distance DIET. [Google Scholar]
  54. Liu F, Rotaru A-E, Shrestha PM, Malvankar NS, Nevin KP, Lovley DR. 54.  2015. Magnetite compensates for the lack of a pilin-assoicated c-type cytochrome in extracellular electron exchange. Environ. Microbiol. 17:648–55 [Google Scholar]
  55. Liu X, Tremblay P-L, Malvankar NS, Nevin KP, Lovley DR, Vargas M. 55.  2014. A Geobacter sulfurreducens strain expressing Pseudomonas aeruginosa type IV pili localizes OmcS on pili but is deficient in Fe(III) oxide reduction and current production. Appl. Environ. Microbiol 80:1219–24 [Google Scholar]
  56. Liu Y, Zhang Y, Zhao Z, Ngo HH, Guo W. 56.  et al. 2017. A modeling approach to direct interspecies electron transfer process in anaerobic transformation of ethanol to methane. Environ. Sci. Pollut. Res. 24:855–63 [Google Scholar]
  57. Lovley DR. 57.  2011. Reach out and touch someone: potential impact of DIET (direct interspecies energy transfer) on anaerobic biogeochemistry, bioremediation, and bioenergy. Rev. Environ. Sci. Biotechnol. 10:101–5 [Google Scholar]
  58. Lovley DR. 58.  2011. Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energy Environ. Sci. 4:4896–906 [Google Scholar]
  59. Lovley DR. 59.  2012. Electromicrobiology. Annu. Rev. Microbiol. 66:391–409 [Google Scholar]
  60. Lovley DR. 60.  2012. Long-range electron transport to Fe(III) oxide via pili with metallic-like conductivity. Biochem. Soc. Trans. 40:1186–90 [Google Scholar]
  61. Lovley DR, Nevin KP. 61.  2013. Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr. Opin. Biotechnol. 24:385–90 [Google Scholar]
  62. Lovley DR, Malvankar NS. 62.  2015. Seeing is believing: novel imaging techniques help clarify microbial nanowire structure and function. Environ. Microbiol. 7:2209–15 [Google Scholar]
  63. Lovley DR. 63.  2017. Happy together: microbial communities that hook up to swap electrons. ISME J 11:327–36 [Google Scholar]
  64. Lü F, Luo C, Shao L, He P. 64.  2016. Biochar alleviates combined stress of ammonium and acids by firstly enriching Methanosaeta and then Methanosarcina. Water Res. 90:34–43 [Google Scholar]
  65. Luo C, Lü F, Shao L, He P. 65.  2015. Application of eco-compatible biochar in anaerobic digestion to relieve acid stress and promote the selective colonization of functional microbes. Water Res 68:710–18 [Google Scholar]
  66. Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C. 66.  et al. 2011. Tunable metallic-like conductivity in nanostructured biofilms comprised of microbial nanowires. Nat. Nanotechnol. 6:573–79 [Google Scholar]
  67. Malvankar NS, Lau J, Nevin KP, Franks AE, Tuominen MT, Lovley DR. 67.  2012. Electrical conductivity in a mixed-species biofilm. Appl. Environ. Microbiol. 78:5967–71 [Google Scholar]
  68. Malvankar NS, Lovley DR. 68.  2012. Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. ChemSusChem 5:1039–46 [Google Scholar]
  69. Malvankar NS, Mester T, Tuominen MT, Lovley DR. 69.  2012. Supercapacitors based on c-type cytochromes using conductive nanostructured networks of living bacteria. ChemPhysChem 13:463–68 [Google Scholar]
  70. Malvankar NS, Tuominen MT, Lovley DR. 70.  2012. Biofilm conductivity is a decisive variable for high-current-density Geobacter sulfurreducens microbial fuel cells. Energy Environ. Sci. 5:5790–97 [Google Scholar]
  71. Malvankar NS, Tuominen MT, Lovley DR. 71.  2012. Lack of involvement of c-type cytochromes in long-range electron transport in microbial biofilms and nanowires. Energy Environ. Sci. 5:8651–59 [Google Scholar]
  72. Malvankar NS, Lovley DR. 72.  2014. Microbial nanowires for bioenergy applications. Curr. Opin. Biotechnol. 27:88–95 [Google Scholar]
  73. Malvankar NS, Yalcin SE, Tuominen MT, Lovley DR. 73.  2014. Visualization of charge propagation along individual pili proteins using ambient electrostatic force microscopy. Nat. Nanotechnol. 9:1012–17 [Google Scholar]
  74. Malvankar NS, Vargas M, Nevin KP, Tremblay P-L, Evans-Lutterodt K. 74.  et al. 2015. Structural basis for metallic-like conductivity in microbial nanowires. mBio 6:e00084–15 [Google Scholar]
  75. McGlynn SE, Chadwick GL, Kempes CP, Orphan VJ. 75.  2015. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526:531–35 [Google Scholar]
  76. McInerney MJ, Sieber JR, Gunsalus RP. 76.  2009. Syntrophy in anaerobic global carbon cycles. Curr. Opin. Biotechnol. 20:623–32 [Google Scholar]
  77. Mehta T, Coppi MV, Childers SE, Lovley DR. 77.  2005. Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol 71:8634–41 [Google Scholar]
  78. Meyerdierks A, Kube M, Lombardot T, Knittel K, Bauer M. 78.  et al. 2005. Insights into the genomes of archaea mediating the anaerobic oxidation of methane. Environ. Microbiol. 7:1937–51This work first suggested that anaerobic methane oxidizers employ cytochromes for interspecies electron exchange. [Google Scholar]
  79. Morita M, Malvankar NS, Franks AE, Summers ZM, Giloteaux L. 79.  et al. 2011. Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. mBio 2:e00159–11 [Google Scholar]
  80. Moscoviz R, Toledo-Alarcon J, Trably E, Bernet N. 80.  2016. Electro-fermentation: how to drive fermentation using electrochemical systems. Trends Biotechnol 34:856–65 [Google Scholar]
  81. Nagarajan H, Embree M, Rotaru A-E, Shrestha PM, Feist AM. 81.  et al. 2013. Multi-omic characterization and modeling of interspecies electron transfer mechanisms and microbial community dynamics of syntrophic associations. Nat. Commun. 4:2809 [Google Scholar]
  82. Nevin KP, Kim B-C, Glaven RH, Johnson JP, Woodard TL. 82.  et al. 2009. Anode biofilm transcriptomics reveals outer surface components essential for high currency power production in Geobacter sulfurreducens fuel cells. PLOS ONE 4:e5628 [Google Scholar]
  83. Oren A. 83.  2014. The family Methanotrichaceae. The Prokaryotes: Other Major Lineages of Bacteria and the Archaea E Rosenberg, EF DeLong, S Lory, E Stackebrandt, F Thompson 297–306 Berlin: Springer-Verlag [Google Scholar]
  84. Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ. 84.  2008. Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. PNAS 105:7052–57 [Google Scholar]
  85. Potter MC. 85.  1910. On the difference of potential due to the vital activity of microorganisms. Proc. Univ. Durham Phil. Soc. 3:245–49 [Google Scholar]
  86. Potter MC. 86.  1911. Electrical effects accompanying the decomposition of organic compounds. Proc. R. Soc. B 84:260–76 [Google Scholar]
  87. Poweleit N, Ge P, Nguyen HN, Loo RRO, Gunsalus RP, Zhou ZH. 87.  2016. CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus. Nat. Microbiol. 2:16222This is an elegant analysis of microbial filament structure. Additional studies like this one are needed to better understand DIET mechanisms. [Google Scholar]
  88. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR. 88.  2005. Extracellular electron transfer via microbial nanowires. Nature 435:1098–101 [Google Scholar]
  89. Reguera G, Nevin KP, Nicoll JS, Covalla SF, Woodard TL, Lovley DR. 89.  2006. Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl. Environ. Microbiol. 72:7345–48 [Google Scholar]
  90. Richter H, Nevin KP, Jia H, Lowy DA, Lovley DR, Tender LM. 90.  2009. Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer. Energy Environ. Sci. 2:506–16 [Google Scholar]
  91. Rosenbaum MA, Franks AE. 91.  2014. Microbial catalysis in bioelectrochemical technologies: status quo, challenges and perspectives. Appl. Microbiol. Biotechnol. 98:509–18 [Google Scholar]
  92. Rotaru A-E, Shrestha PM, Liu A, Ueki T, Nevin KP, Lovley DR. 92.  2012. Interspecies electron transfer via H2 and formate rather than direct electrical connections in co-cultures of Pelobacter carbinolicus and Geobacter sulfurreducens. Appl. Environ. Microbiol. 78:7645–51 [Google Scholar]
  93. Rotaru A-E, Shrestha PM, Liu F, Nevin KP, Lovley DR. 93.  2014. Direct interspecies electron transfer during syntrophic growth of Geobacter metallireducens and Methanosarcina barkeri on ethanol. Appl. Environ. Microbiol 80:4599–605 [Google Scholar]
  94. Rotaru A-E, Shrestha PM, Liu F, Shrestha M, Shrestha D. 94.  et al. 2014. A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ. Sci. 7:408–15The first demonstration of DIET in complex communities and the participation of archaea in DIET are shown in this study. [Google Scholar]
  95. Rotaru A-E, Woodard TL, Nevin KP, Lovley DR. 95.  2015. Link between capacity for current production and syntrophic growth in Geobacter species. Front. Microbiol. 6:744 [Google Scholar]
  96. Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ. 96.  2016. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351:703–7 [Google Scholar]
  97. Shi L, Dong H, Reguera G, Beyenal H, Lu A. 97.  et al. 2016. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14:651–62This is an excellent comprehensive review on mechanisms for extracellular electron exchange. [Google Scholar]
  98. Shi L, Tien M, Fredrickson JK, Zachara JM, Rosso KM. 98.  2016. Microbial redox proteins and protein complexes for extracellular respiration. Redox Proteins in Supercomplexes and Signalosomes RO Louro, I Diaz-Moreno 187–216 New York: CRC Press [Google Scholar]
  99. Shrestha PM, Rotaru A-E, Aklujkar M, Liu F, Shrestha M. 99.  et al. 2013. Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. Environ. Microbiol. Rep. 5:904–10 [Google Scholar]
  100. Shrestha PM, Rotaru A-E, Summers ZM, Shrestha M, Liu F, Lovley DR. 100.  2013. Transcriptomic and genetic analysis of direct interspecies electron transfer. Appl. Environ. Microbiol. 79:2397–404 [Google Scholar]
  101. Shrestha PM, Malvankar NS, Werner JJ, Franks AE, Rotaru A-E. 101.  et al. 2014. Correlation between microbial community and granule conductivity in anaerobic bioreactors for brewery wastewater treatment. Bioresour. Technol. 174:306–10 [Google Scholar]
  102. Smith JA, Lovley DR, Tremblay PL. 102.  2013. Outer cell surface components essential for Fe(III) oxide reduction by Geobacter metallireducens. Appl. Environ. Microbiol. 79:901–7 [Google Scholar]
  103. Smith JA, Nevin KP, Lovley DR. 103.  2015. Syntrophic growth via quinone-mediated interspecies electron transfer. Front. Microbiol. 6:121 [Google Scholar]
  104. Smith KS, Ingram-Smith C. 104.  2007. Methanosaeta, the forgotten methanogen?. Trends Microbiol 15:150–55 [Google Scholar]
  105. Song H-K, Sonkaria S, Khare V, Dong K, Lee H-T. 105.  et al. 2015. Pond sediment magnetite grains show a distinctive microbial community. Microb. Ecol. 70:168–74 [Google Scholar]
  106. Stams AJ, Plugge CM. 106.  2009. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7:568–77 [Google Scholar]
  107. Storck T, Virdis B, Batstone DJ. 107.  2015. Modelling extracellular limitations for mediated versus direct interspecies electron transfer. ISME J 10:621–31 [Google Scholar]
  108. Strycharz SM, Malanoski AP, Snider RM, Yi H, Lovley DR, Tender LM. 108.  2011. Application of cyclic voltammetry to investigate enhanced catalytic current generation by biofilm-modified anodes of Geobacter sulfurreducens strain DL1 versus variant strain KN400. Energy Environ. Sci. 4:896–913 [Google Scholar]
  109. Summers ZM, Fogarty H, Leang C, Franks AE, Malvankar NS, Lovley DR. 109.  2010. Direct exchange of electrons within aggregates of an evolved syntrophic co-culture of anaerobic bacteria. Science 330:1413–15This work summarizes the experiments that led to the discovery of direct interspecies electron transfer. [Google Scholar]
  110. Sure S, Ackland ML, Torriero AJ, Adholeya A, Kochar M. 110.  2016. Microbial nanowires: an electrifying tale. Microbiology 162:2017–28 [Google Scholar]
  111. Tan Y, Adhikari RY, Malvankar NS, Pi S, Ward JE. 111.  et al. 2016. Synthetic biological protein nanowires with high conductivity. Small 12:4481–85 [Google Scholar]
  112. Tan Y, Adhikari RY, Malvankar NS, Ward JE, Nevin KP. 112.  et al. 2016. The low conductivity of Geobacter uraniireducens pili suggests a diversity of extracellular electron transfer mechanisms in the genus Geobacter. Front. Microbiol. 7:980 [Google Scholar]
  113. Tan Y, Adhikari RY, Malvankar NS, Ward JE, Woodard TL. 113.  et al. 2017. Expressing the Geobacter metallireducens PilA in Geobacter sulfurreducens yields pili with exceptional conductivity. mBio 8:e02203–16 [Google Scholar]
  114. Tang J, Zhuang L, Ma J, Tang Z, Yu Z, Zhou S. 114.  2016. Secondary mineralization of ferrihydrite affects microbial methanogenesis in Geobacter-Methanosarcina cocultures. Appl. Environ. Microbiol 82:5869–77 [Google Scholar]
  115. Timmers PHA, Welte CU, Koehorst JJ, Plugge CM, Jetten MSM, Stams AJM. 115.  2017. Reverse methanogenesis and respiration in methanotrophic archaea. Archaea 2017:1654237 [Google Scholar]
  116. Trembath-Reichert E, Case DH, Orphan VJ. 116.  2016. Characterization of microbial associations with methanotrophic archaea and sulfate-reducing bacteria through statistical comparison of nested Magneto-FISH enrichments. PeerJ 4:e1913 [Google Scholar]
  117. Tveit AT, Urich T, Frenzel P, Svenning MM. 117.  2015. Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming. PNAS 112:E2507–16 [Google Scholar]
  118. Vargas M, Malvankar NS, Tremblay P-L, Leang C, Smith JA. 118.  et al. 2013. Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio 4:e00105–13 [Google Scholar]
  119. Venkidusamy K, Megharah M, Schroder U, Karouta F, Mohan SV, Naidu R. 119.  2015. Electron transport through electrically conductive nanofilaments in Rhodopseudomonas palustris strain RP2. RSC Adv 5:100790–98 [Google Scholar]
  120. Viggi CC, Rossetti S, Fazi S, Paiano P, Majone M, Aulenta F. 120.  2014. Magnetite particles triggering a faster and more robust syntrophic pathway of methanogenic propionate degradation. Environ. Sci. Technol. 48:7536–43 [Google Scholar]
  121. Walker DJF, Adhikari RY, Holmes DE, Ward JE, Woodard TL. 121.  et al. 2017. Electrically conductive pili from genes of phylogenetically diverse microorganisms. bioRxiv 118059 https://doi.org/10.1101/118059 [Crossref]
  122. Wang L-Y, Nevin KP, Woodard TL, Mu B-Z, Lovley DR. 122.  2016. Expanding the diet for DIET: electron donors supporting direct interspecies electron transfer (DIET) in defined co-cultures. Front. Microbiol. 7:236 [Google Scholar]
  123. Wegener G, Krukenberg V, Riedel D, Tegetmeyer HE, Boetius A. 123.  2015. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526:587–90This study offers an interesting hypothesis that conductive filaments may wire together an anaerobic methane oxidation community for DIET. [Google Scholar]
  124. Xiao K, Malvankar NS, Shu C, Martz E, Lovley DR, Sun X. 124.  2016. Low energy atomic models suggesting a pilus structure that could account for electrical conductivity along the length of Geobacter sulfurreducens pili. Sci. Rep. 6:23385 [Google Scholar]
  125. Yamada C, Kato S, Ueno Y, Ishii M, Igarashi Y. 125.  2015. Conductive iron oxides accelerate thermophilic methanogenesis from acetate and propionate. J. Biosci. Bioeng. 119:678–82 [Google Scholar]
  126. Yun J, Malvankar NS, Ueki T, Lovley DR. 126.  2016. Functional environmental proteomics: elucidating the role of a c-type cytochrome abundant during uranium bioremediation. ISME J 10:310–20 [Google Scholar]
  127. Zhang J, Lu Y. 127.  2016. Conductive Fe3O4 nanoparticles accelerate syntrophic methane production from butyrate oxidation in two different lake sediments. Front. Microbiol. 7:1316 [Google Scholar]
  128. Zhao Z, Zhang Y, Woodard TL, Nevin KP, Lovley DR. 128.  2015. Enhancing syntrophic metabolism in up-flow anaerobic sludge blanket reactors with conductive carbon materials. Bioresour. Technol. 191:140–45 [Google Scholar]
  129. Zhao Z, Zhang Y, Li Y, Dang Y, Zhu T, Quan X. 129.  2017. Potentially shifting from interspecies hydrogen transfer to direct interspecies electron transfer for syntrophic metabolism to resist acidic impact with conductive carbon cloth. Chem. Eng. J. 313:10–18 [Google Scholar]
  130. Zhao Z, Zhang Y, Yu Q, Dang Y, Li Y, Quan X. 130.  2016. Communities stimulated with ethanol to perform direct interspecies electron transfer for syntrophic metabolism of propionate and butyrate. Water Res 102:475–84 [Google Scholar]
  131. Zhuang L, Tang J, Wang Y, Hu M, Zhou S. 131.  2015. Conductive iron oxide minerals accelerate syntrophic cooperation in methanogenic benzoate degradation. J. Hazard. Mater. 293:37–45 [Google Scholar]
  132. Zhuang L, Ma J, Tang J, Tang Z, Zhou S. 132.  2017. Cysteine-accelerated methanogenic propionate degradation in paddy soil enrichment. Microb. Ecol. 73:916–24 [Google Scholar]
/content/journals/10.1146/annurev-micro-030117-020420
Loading
Syntrophy Goes Electric: Direct Interspecies Electron Transfer
Annual Review of Microbiology 71, 643 (2017); https://doi.org/10.1146/annurev-micro-030117-020420
/content/journals/10.1146/annurev-micro-030117-020420
/content/journals/10.1146/annurev-micro-030117-020420
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error