Descriptions of the changeable, striking colors associated with secreted natural products date back well over a century. These molecules can serve as extracellular electron shuttles (EESs) that permit microbes to access substrates at a distance. In this review, we argue that the colorful world of EESs has been too long neglected. Rather than simply serving as a diagnostic attribute of a particular microbial strain, redox-active natural products likely play fundamental, underappreciated roles in the biology of their producers, particularly those that inhabit biofilms. Here, we describe the chemical diversity and potential distribution of EES producers and users, discuss the costs associated with their biosynthesis, and critically evaluate strategies for their economical usage. We hope this review will inspire efforts to identify and explore the importance of EES cycling by a wide range of microorganisms so that their contributions to shaping microbial communities can be better assessed and exploited.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. 1. Chemnetbase. 2017. Dictionary of Natural Products 25.2, Taylor and Francis, Oxford, UK, accessed February 2017. http://dnp.chemnetbase.com/
  2. Alberty RA. 2.  1994. Thermodynamics of the nitrogenase reactions. J. Biol. Chem. 269:7099–102 [Google Scholar]
  3. Amthor JS. 3.  2000. The McCree–de Wit–Penning de Vries–Thornley respiration paradigms: 30 years later. Ann. Bot. 86:1–20 [Google Scholar]
  4. Assary RS, Brushett FR, Curtiss LA. 4.  2014. Reduction potential predictions of some aromatic nitrogen-containing molecules. RSC Adv 4:57442–51 [Google Scholar]
  5. Bacher A, Eberhardt S, Fischer M, Kis K, Richter G. 5.  2000. Biosynthesis of vitamin B2 (riboflavin). Annu. Rev. Nutr. 20:153–67 [Google Scholar]
  6. Baran R, Ivanova NN, Jose N, Garcia-Pichel F, Kyrpides NC. 6.  et al. 2013. Functional genomics of novel secondary metabolites from diverse cyanobacteria using untargeted metabolomics. Mar. Drugs 11:3617–31 [Google Scholar]
  7. Benz M, Schink B, Brune A. 7.  1998. Humic acid reduction by Propionibacterium freudenreichii and other fermenting bacteria. Appl. Environ. Microbiol. 64:4507–12 [Google Scholar]
  8. Bergkessel M, Basta DW, Newman DK. 8.  2016. The physiology of growth arrest: uniting molecular and environmental microbiology. Nat. Rev. Microbiol. 14:549–62 [Google Scholar]
  9. Blankenfeldt W, Parsons JF. 9.  2014. The structural biology of phenazine biosynthesis. Curr. Opin. Struct. Biol. 29:26–33 [Google Scholar]
  10. Blauch DN, Saveant JM. 10.  1992. Dynamics of electron hopping in assemblies of redox centers. Percolation and diffusion. J. Am. Chem. Soc. 114:3323–32 [Google Scholar]
  11. Bond DR, Lovley DR. 11.  2005. Evidence for involvement of an electron shuttle in electricity generation by Geothrix fermentans. Appl. Environ. Microbiol. 71:2186–89 [Google Scholar]
  12. Boyd DA, Erickson JS, Roy JN, Snider RM, Strycharz-Glaven SM, Tender LM. 12.  2015. Theory of redox conduction and the measurement of electron transport rates through electrochemically active biofilms. Biofilms in Bioelectrochemical Systems: From Laboratory Practice to Data Interpretation H Beyenal, JT Babauta 177–210 Hoboken, NJ: Wiley [Google Scholar]
  13. Brutinel ED, Gralnick JA. 13.  2012. Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl. Microbiol. Biotechnol. 93:41–48 [Google Scholar]
  14. Chen I-MA, Markowitz VM, Chu K, Palaniappan K, Szeto E. 14.  et al. 2016. IMG/M: integrated genome and metagenome comparative data analysis system. Nucleic Acids Res 45:D507–16 [Google Scholar]
  15. Coates JD, Cole KA, Chakraborty R, O'Connor SM, Achenbach LA. 15.  2002. Diversity and ubiquity of bacteria capable of utilizing humic substances as electron donors for anaerobic respiration. Appl. Environ. Microbiol. 68:2445–52 [Google Scholar]
  16. Coates JD, Ellis DJ, Blunt-Harris EL, Gaw CV, Roden EE, Lovley DR. 16.  1998. Recovery of humic-reducing bacteria from a diversity of environments. Appl. Environ. Microbiol. 64:1504–9 [Google Scholar]
  17. Cobb RE, Wang Y, Zhao H. 17.  2014. High-efficiency multiplex genome editing of Streptomyces species using an engineered CRISPR/Cas system. ACS Synth. Biol. 4:723–28 [Google Scholar]
  18. Cochemé HM, Murphy MP. 18.  2008. Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem. 283:1786–98 [Google Scholar]
  19. Conn JE. 19.  1943. The pigment production of Actinomyces coelicolor. A. violaceus-ruber. J. Bacteriol. 46:133 [Google Scholar]
  20. Costa KC, Bergkessel M, Saunders S, Korlach J, Newman DK. 20.  2015. Enzymatic degradation of phenazines can generate energy and protect sensitive organisms from toxicity. mBio 6:e01520–15 [Google Scholar]
  21. Costa KC, Glasser NR, Conway SJ, Newman DK. 21.  2017. Pyocyanin degradation by a tautomerizing demethylase inhibits Pseudomonas aeruginosa biofilms. Science 355:170–73 [Google Scholar]
  22. Cowley ES, Kopf SH, LaRiviere A, Ziebis W, Newman DK. 22.  2015. Pediatric cystic fibrosis sputum can be chemically dynamic, anoxic, and extremely reduced due to hydrogen sulfide formation. mBio 6:e00767–15 [Google Scholar]
  23. Cruz RD, Gao Y, Penumetcha S, Sheplock R, Weng K, Chander M. 23.  2010. Expression of the Streptomyces coelicolor SoxR regulon is intimately linked with actinorhodin production. J. Bacteriol. 192:6428–38 [Google Scholar]
  24. Cude WN, Mooney J, Tavanaei AA, Hadden MK, Frank AM. 24.  et al. 2012. Production of the antimicrobial secondary metabolite indigoidine contributes to competitive surface colonization by the marine roseobacter Phaeobacter sp. strain Y4I. Appl. Environ. Microbiol. 78:4771–80 [Google Scholar]
  25. Das T, Kutty SK, Tavallaie R, Ibugo AI, Panchompoo J. 25.  et al. 2015. Phenazine virulence factor binding to extracellular DNA is important for Pseudomonas aeruginosa biofilm formation. Sci. Rep. 5:8398 [Google Scholar]
  26. Das T, Manefield M. 26.  2012. Pyocyanin promotes extracellular DNA release in Pseudomonas aeruginosa. PLOS ONE 7:e46718 [Google Scholar]
  27. Deng L, Li F, Zhou S, Huang D, Ni J. 27.  2010. A study of electron-shuttle mechanism in Klebsiella pneumoniae based-microbial fuel cells. Chin. Sci. Bull. 55:99–104 [Google Scholar]
  28. Dewick PM. 28.  1994. The biosynthesis of shikimate metabolites. Nat. Prod. Rep. 11:173–203 [Google Scholar]
  29. Dhall S, Do DC, Garcia M, Kim J, Mirebrahim SH. 29.  et al. 2014. Generating and reversing chronic wounds in diabetic mice by manipulating wound redox parameters. J. Diabetes Res. 2014:562625 [Google Scholar]
  30. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK. 30.  2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61:1308–21 [Google Scholar]
  31. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK. 31.  2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61:1308–21 [Google Scholar]
  32. Dietrich LEP, Okegbe C, Price-Whelan A, Sakhtah H, Hunter RC, Newman DK. 32.  2013. Bacterial community morphogenesis is intimately linked to the intracellular redox state. J. Bacteriol. 195:1371–80 [Google Scholar]
  33. Dietrich LEP, Teal TK, Price-Whelan A, Newman DK. 33.  2008. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203–6 [Google Scholar]
  34. Diggle SP, Griffin AS, Campbell GS, West SA. 34.  2007. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:411–14 [Google Scholar]
  35. Emde R, Swain A, Schink B. 35.  1989. Anaerobic oxidation of glycerol by Escherichia coli in an amperometric poised-potential culture system. Appl. Microbiol. Biotechnol. 32:170–75 [Google Scholar]
  36. Farrington JA, Ebert M, Land EJ, Fletcher K. 36.  1973. Bipyridylium quaternary salts and related compounds. V. Pulse radiolysis studies of the reaction of paraquat radical with oxygen. Implications for the mode of action of bipyridyl herbicides. Biochim. Biophys. Acta Bioenerg. 314:372–81 [Google Scholar]
  37. Federhen S. 37.  2012. The NCBI taxonomy database. Nucleic Acids Res 40:D136–43 [Google Scholar]
  38. Freguia S, Masuda M, Tsujimura S, Kano K. 38.  2009. Lactococcus lactis catalyses electricity generation at microbial fuel cell anodes via excretion of a soluble quinone. Bioelectrochemistry 76:14–18 [Google Scholar]
  39. Friedheim E, Michaelis L. 39.  1931. Potentiometric study of pyocyanine. J. Biol. Chem. 91:355–68 [Google Scholar]
  40. Fuller SJ, McMillan DG, Renz MB, Schmidt M, Burke IT, Stewart DI. 40.  2014. Extracellular electron transport-mediated Fe(III) reduction by a community of alkaliphilic bacteria that use flavins as electron shuttles. Appl. Environ. Microbiol. 80:128–37 [Google Scholar]
  41. Galkin AS, Grivennikova VG, Vinogradov AD. 41.  1999. →H+/2e stoichiometry in NADH-quinone reductase reactions catalyzed by bovine heart submitochondrial particles. FEBS Lett 451:157–61 [Google Scholar]
  42. Garrity GM, Bell JA, Lilburn TG. 42.  2004. Taxonomic Outline of the Prokaryotes. Bergey's Manual of Systematic Bacteriology New York: Springer
  43. Gauthier M, Flatau G. 43.  1976. Antibacterial activity of marine violet-pigmented Alteromonas with special reference to the production of brominated compounds. Can. J. Microbiol. 22:1612–19 [Google Scholar]
  44. Gerstel U, Römling U. 44.  2001. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ. Microbiol. 3:638–48 [Google Scholar]
  45. Glasser NR, Kern SE, Newman DK. 45.  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 [Google Scholar]
  46. Glasser NR, Wang BX, Hoy JA, Newman DK. 46.  2017. The pyruvate and α-ketoglutarate dehydrogenase complexes of Pseudomonas aeruginosa catalyze pyocyanin and phenazine-1-carboxylic acid reduction via the subunit dihydrolipoamide dehydrogenase. J. Biol. Chem. 292:5593–607 [Google Scholar]
  47. Glick R, Gilmour C, Tremblay J, Satanower S, Avidan O. 47.  et al. 2010. Increase in rhamnolipid synthesis under iron-limiting conditions influences surface motility and biofilm formation in Pseudomonas aeruginosa. J. Bacteriol. 192:2973–80 [Google Scholar]
  48. Grahl N, Kern SE, Newman DK, Hogan DA. 48.  2013. The yin and the yang of phenazine physiology. Microbial Phenazines: Biosynthesis, Agriculture and Health S Chincholkar, L Thomashow 43–70 Heidelberg, Ger.: Springer [Google Scholar]
  49. Gray HB, Winkler JR. 49.  1996. Electron transfer in proteins. Annu. Rev. Biochem. 65:537–61 [Google Scholar]
  50. Griffin AS, West SA, Buckling A. 50.  2004. Cooperation and competition in pathogenic bacteria. Nature 430:1024–27 [Google Scholar]
  51. Hadjithomas M, Chen I-MA, Chu K, Ratner A, Palaniappan K. 51.  et al. 2015. IMG-ABC: a knowledge base to fuel discovery of biosynthetic gene clusters and novel secondary metabolites. mBio 6:e00932–15 [Google Scholar]
  52. Hassan HM, Fridovich I. 52.  1979. Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds. Arch. Biochem. Biophys. 196:385–95 [Google Scholar]
  53. Hense BA, Kuttler C, Müller J, Rothballer M, Hartmann A, Kreft J-U. 53.  2007. Does efficiency sensing unify diffusion and quorum sensing?. Nat. Rev. Microbiol. 5:230–39 [Google Scholar]
  54. Hernandez ME, Kappler A, Newman DK. 54.  2004. Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl. Environ. Microbiol. 70:921–28 [Google Scholar]
  55. Hernandez ME, Newman DK. 55.  2001. Extracellular electron transfer. Cell. Mol. Life Sci. 58:1562–71 [Google Scholar]
  56. Herrmann G, Jayamani E, Mai G, Buckel W. 56.  2008. Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J. Bacteriol. 199:784–91 [Google Scholar]
  57. 57. Hum. Microbiome Proj. Consort. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207–14 [Google Scholar]
  58. Hunter RC, Klepac-Ceraj V, Lorenzi MM, Grotzinger H, Martin TR, Newman DK. 58.  2012. Phenazine content in the cystic fibrosis respiratory tract negatively correlates with lung function and microbial complexity. Am. J. Respir. Cell Mol. Biol. 47:738–45 [Google Scholar]
  59. Jelen BI, Giovannelli D, Falkowski PG. 59.  2016. The role of microbial electron transfer in the coevolution of the biosphere and geosphere. Annu. Rev. Microbiol. 70:45–62 [Google Scholar]
  60. Jiang J, Kappler A. 60.  2008. Kinetics of microbial and chemical reduction of humic substances: implications for electron shuttling. Environ. Sci. Technol. 42:3563–69 [Google Scholar]
  61. Kappler A, Benz M, Schink B, Brune A. 61.  2004. Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment. FEMS Microbiol. Ecol. 47:85–92 [Google Scholar]
  62. Kappler A, Haderlein SB. 62.  2003. Natural organic matter as reductant for chlorinated aliphatic pollutants. Environ. Sci. Technol. 37:2714–19 [Google Scholar]
  63. Keck A, Rau J, Reemtsma T, Mattes R, Stolz A, Klein J. 63.  2002. Identification of quinoide redox mediators that are formed during the degradation of naphthalene-2-sulfonate by Sphingomonas xenophaga BN6. Appl. Environ. Microbiol. 68:4341–49 [Google Scholar]
  64. Kempes CP, Okegbe C, Mears-Clarke Z, Follows MJ, Dietrich LE. 64.  2014. Morphological optimization for access to dual oxidants in biofilms. PNAS 111:208–13 [Google Scholar]
  65. Khan MT, Duncan SH, Stams AJ, van Dijl JM, Flint HJ, Harmsen HJ. 65.  2012. The gut anaerobe Faecalibacterium prausnitzii uses an extracellular electron shuttle to grow at oxic–anoxic interphases. ISME J 6:1578–85 [Google Scholar]
  66. Kotloski NJ, Gralnick JA. 66.  2013. Flavin electron shuttles dominate extracellular electron transfer by Shewanella oneidensis. mBio 4:e00553–12 [Google Scholar]
  67. Kümmerli R, Schiessl KT, Waldvogel T, McNeill K, Ackermann M. 67.  2014. Habitat structure and the evolution of diffusible siderophores in bacteria. Ecol. Lett. 17:1536–44 [Google Scholar]
  68. Lee A, Newman D. 68.  2003. Microbial iron respiration: impacts on corrosion processes. Appl. Microbiol. Biotechnol. 62:134–39 [Google Scholar]
  69. Letunic I, Bork P. 69.  2016. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–45 [Google Scholar]
  70. Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W, Thauer RK. 70.  2008. Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J. Bacteriol. 190:843–50 [Google Scholar]
  71. Lies DP, Hernandez ME, Kappler A, Mielke RE, Gralnick JA, Newman DK. 71.  2005. Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for biofilms. Appl. Environ. Microbiol. 71:4414–26 [Google Scholar]
  72. Lovley DR. 72.  2006. Bug juice: harvesting electricity with microorganisms. Nat. Rev. Microbiol. 4:497–508 [Google Scholar]
  73. Lukacs GL, Haggie P, Seksek O, Lechardeur D, Freedman N, Verkman A. 73.  2000. Size-dependent DNA mobility in cytoplasm and nucleus. J. Biol. Chem. 275:1625–29 [Google Scholar]
  74. Malvankar NS, Rotello VM, Tuominen MT, Lovley DR. 74.  2016. Reply to ‘Measuring conductivity of living Geobacter sulfurreducens biofilms’. Nat. Nanotechnol. 11:913–14 [Google Scholar]
  75. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR. 75.  2008. Shewanella secretes flavins that mediate extracellular electron transfer. PNAS 105:3968–73 [Google Scholar]
  76. McGlynn SE, Chadwick GL, Kempes CP, Orphan VJ. 76.  2015. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526:531–35 [Google Scholar]
  77. Murray AG, Jackson GA. 77.  1992. Viral dynamics: a model of the effects of size, shape, motion and abundance of single-celled planktonic organisms and other particles. Mar. Ecol. Prog. Ser. Oldendorf 89:103–16 [Google Scholar]
  78. Nadell CD, Xavier JB, Foster KR. 78.  2009. The sociobiology of biofilms. FEMS Microbiol. Rev. 33:206–24 [Google Scholar]
  79. Nauman JV, Campbell PG, Lanni F, Anderson JL. 79.  2007. Diffusion of insulin-like growth factor-I and ribonuclease through fibrin gels. Biophys. J. 92:4444–50 [Google Scholar]
  80. Neilands J. 80.  1981. Iron absorption and transport in microorganisms. Annu. Rev. Nutr. 1:27–46 [Google Scholar]
  81. O'Toole G, Kaplan HB, Kolter R. 81.  2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49–79 [Google Scholar]
  82. Palma M, Zurita J, Ferreras JA, Worgall S, Larone DH. 82.  et al. 2005. Pseudomonas aeruginosa SoxR does not conform to the archetypal paradigm for SoxR-dependent regulation of the bacterial oxidative stress adaptive response. Infect. Immun. 73:2958–66 [Google Scholar]
  83. Pence HE, Williams A. 83.  2010. ChemSpider: an online chemical information resource. J. Chem. Educ. 87:1123–24 [Google Scholar]
  84. Peters JM, Silvis MR, Zhao D, Hawkins JS, Gross CA, Qi LS. 84.  2015. Bacterial CRISPR: accomplishments and prospects. Curr. Opin. Microbiol. 27:121–26 [Google Scholar]
  85. Petrauskas AA, Kolovanov EA. 85.  2000. ACD/Log P method description. Perspect. Drug Discov. Des. 19:99–116 [Google Scholar]
  86. Pfeffer C, Larsen S, Song J, Dong M, Besenbacher F. 86.  et al. 2012. Filamentous bacteria transport electrons over centimetre distances. Nature 491:218–21 [Google Scholar]
  87. Phalak P, Chen J, Carlson RP, Henson MA. 87.  2016. Metabolic modeling of a chronic wound biofilm consortium predicts spatial partitioning of bacterial species. BMC Syst. Biol. 10:90 [Google Scholar]
  88. Phan H, Yates MD, Kirchhofer ND, Bazan GC, Tender LM, Nguyen T-Q. 88.  2016. Biofilm as a redox conductor: a systematic study of the moisture and temperature dependence of its electrical properties. Phys. Chem. Chem. Phys. 18:17815–21 [Google Scholar]
  89. Picioreanu C, Head IM, Katuri KP, van Loosdrecht MC, Scott K. 89.  2007. A computational model for biofilm-based microbial fuel cells. Water Res 41:2921–40 [Google Scholar]
  90. Pierson LS III, Thomashow LS. 90.  1992. Cloning and heterologous expression of the phenazine biosynthetic. Mol. Plant-Microbe Interact. 5:330–39 [Google Scholar]
  91. Pirbadian S, El-Naggar MY. 91.  2012. Multistep hopping and extracellular charge transfer in microbial redox chains. Phys. Chem. Chem. Phys. 14:13802–8 [Google Scholar]
  92. Pomposiello PJ, Demple B. 92.  2001. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 19:109–14 [Google Scholar]
  93. Price-Whelan A, Dietrich LE, Newman DK. 93.  2006. Rethinking ‘secondary’ metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2:71–78 [Google Scholar]
  94. Price-Whelan A, Dietrich LE, Newman DK. 94.  2007. Pyocyanin alters redox homeostasis and carbon flux through central metabolic pathways in Pseudomonas aeruginosa PA14. J. Bacteriol. 189:6372–81 [Google Scholar]
  95. Ramos I, Dietrich LE, Price-Whelan A, Newman DK. 95.  2010. Phenazines affect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales. Res. Microbiol. 161:187–91 [Google Scholar]
  96. Redfield RJ. 96.  2002. Is quorum sensing a side effect of diffusion sensing?. Trends Microbiol 10:365–70 [Google Scholar]
  97. Robuschi L, Tomba JP, Schrott GD, Bonanni PS, Desimone PM, Busalmen JP. 97.  2013. Spectroscopic slicing to reveal internal redox gradients in electricity‐producing biofilms. Angew. Chem. Int. Ed. 52:925–28 [Google Scholar]
  98. Roden EE, Kappler A, Bauer I, Jiang J, Paul A. 98.  et al. 2010. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat. Geosci. 3:417–21 [Google Scholar]
  99. Rosso KM, Smith DM, Wang Z, Ainsworth CC, Fredrickson JK. 99.  2004. Self-exchange electron transfer kinetics and reduction potentials for anthraquinone disulfonate. J. Phys. Chem. A 108:3292–303 [Google Scholar]
  100. Sakhtah H, Koyama L, Zhang Y, Morales DK, Fields BL. 100.  et al. 2016. The Pseudomonas aeruginosa efflux pump MexGHI-OpmD transports a natural phenazine that controls gene expression and biofilm development. PNAS 113:E3538–47 [Google Scholar]
  101. Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ. 101.  2016. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351:703–7 [Google Scholar]
  102. Schertzer JW, Boulette ML, Whiteley M. 102.  2009. More than a signal: non-signaling properties of quorum sensing molecules. Trends Microbiol 17:189–95 [Google Scholar]
  103. Schuster M, Sexton DJ, Diggle SP, Greenberg EP. 103.  2013. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu. Rev. Microbiol. 67:43–63 [Google Scholar]
  104. Scott DT, McKnight DM, Blunt-Harris EL, Kolesar SE, Lovley DR. 104.  1998. Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ. Sci. Technol. 32:2984–89 [Google Scholar]
  105. Shi L, Dong H, Reguera G, Beyenal H, Lu A. 105.  et al. 2016. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14:651–62 [Google Scholar]
  106. Shi L, Rosso KM, Clarke TA, Richardson DJ, Zachara JM, Fredrickson JK. 106.  2012. Molecular underpinnings of Fe(III) oxide reduction by Shewanella oneidensis MR-1. Front. Microbiol. 3:46–55 [Google Scholar]
  107. Silva LP, Northen TR. 107.  2015. Exometabolomics and MSI: deconstructing how cells interact to transform their small molecule environment. Curr. Opin. Biotechnol. 34:209–16 [Google Scholar]
  108. Singh AK, Shin JH, Lee KL, Imlay JA, Roe JH. 108.  2013. Comparative study of SoxR activation by redox‐active compounds. Mol. Microbiol. 90:983–96 [Google Scholar]
  109. Smith JA, Tremblay P-L, Shrestha PM, Snoeyenbos-West OL, Franks AE. 109.  et al. 2014. Going wireless: Fe(III) oxide reduction without pili by Geobacter sulfurreducens strain JS-1. Appl. Environ. Microbiol. 80:4331–40 [Google Scholar]
  110. Snider RM, Strycharz-Glaven SM, Tsoi SD, Erickson JS, Tender LM. 110.  2012. Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven. PNAS 109:15467–72 [Google Scholar]
  111. Stewart PS. 111.  2003. Diffusion in biofilms. J. Bacteriol. 185:1485–91 [Google Scholar]
  112. Stewart PS, Franklin MJ. 112.  2008. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6:199–210 [Google Scholar]
  113. Strycharz-Glaven SM, Snider RM, Guiseppi-Elie A, Tender LM. 113.  2011. On the electrical conductivity of microbial nanowires and biofilms. Energy Environ. Sci. 4:4366–79 [Google Scholar]
  114. Subramanian P, Pirbadian S, El-Naggar MY, Jensen GJ. 114.  2017. The ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryo-tomography. bioRxiv 103242. https://doi.org/10.1101/103242 [Crossref]
  115. Sullivan NL, Tzeranis DS, Wang Y, So PT, Newman D. 115.  2011. Quantifying the dynamics of bacterial secondary metabolites by spectral multiphoton microscopy. ACS Chem. Biol. 6:893–99 [Google Scholar]
  116. Tan Y, Adhikari RY, Malvankar NS, Ward JE, Nevin KP. 116.  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]
  117. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, Gordon JI. 117.  2007. The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature 449:804 [Google Scholar]
  118. Uchimiya M, Stone AT. 118.  2009. Reversible redox chemistry of quinones: impact on biogeochemical cycles. Chemosphere 77:451–58 [Google Scholar]
  119. Wang Y, Kern SE, Newman DK. 119.  2010. Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J. Bacteriol. 192:365–69 [Google Scholar]
  120. Wang Y, Newman DK. 120.  2008. Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ. Sci. Technol. 42:2380–86 [Google Scholar]
  121. Wang Y, Wilks JC, Danhorn T, Ramos I, Croal L, Newman DK. 121.  2011. Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J. Bacteriol. 193:3606–17 [Google Scholar]
  122. Weber T, Blin K, Duddela S, Krug D, Kim HU. 122.  et al. 2015. antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237–43 [Google Scholar]
  123. West SA, Griffin AS, Gardner A, Diggle SP. 123.  2006. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4:597–607 [Google Scholar]
  124. Xavier JB, Kim W, Foster KR. 124.  2011. A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol. Microbiol. 79:166–79 [Google Scholar]
  125. Xu KD, Stewart PS, Xia F, Huang CT, McFeters GA. 125.  1998. Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl. Environ. Microbiol. 64:4035–39 [Google Scholar]
  126. Yates MD, Golden JP, Roy J, Strycharz-Glaven SM, Tsoi S. 126.  et al. 2015. Thermally activated long range electron transport in living biofilms. Phys. Chem. Chem. Phys. 17:32564–70 [Google Scholar]
  127. Yates MD, Strycharz-Glaven SM, Golden JP, Roy J, Tsoi S. 127.  et al. 2016. Measuring conductivity of living Geobacter sulfurreducens biofilms. Nat. Nanotechnol. 11:910–13 [Google Scholar]
  128. Yates MD, Strycharz-Glaven SM, Tender LM. 128.  2016. Toward understanding long-distance extracellular electron transport in an electroautotrophic microbial community. Energy Environ. Sci. 9:3544–58 [Google Scholar]
  129. Young G. 129.  1947. Pigment production and antibiotic activity in cultures of Pseudomonas aeruginosa.. J. Bacteriol. 54:109 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
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