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Extracellular Electron Transfer and Biosensors

  • Francesca Simonte
  • Gunnar Sturm
  • Johannes Gescher
  • Katrin Sturm-RichterEmail author
Chapter
Part of the Advances in Biochemical Engineering/Biotechnology book series (ABE, volume 167)

Abstract

This chapter summarizes in the beginning our current understanding of extracellular electron transport processes in organisms belonging to the genera Shewanella and Geobacter. Organisms belonging to these genera developed strategies to transport respiratory electrons to the cell surface that are defined by modules of which some seem to be rather unique for one or the other genus while others are similar. We use this overview regarding our current knowledge of extracellular electron transfer to explain the physiological interaction of microorganisms in direct interspecies electron transfer, a process in which one organism basically comprises the electron acceptor for another microbe and that depends also on extended electron transport chains. This analysis of mechanisms for the transport of respiratory electrons to insoluble electron acceptors ends with an overview of questions that remain so far unanswered. Moreover, we use the description of the biochemistry of extracellular electron transport to explain the fundamentals of biosensors based on this process and give an overview regarding their status of development and applicability.

Graphical Abstract

Keywords

c-type cytochromes Direct interspecies electron transfer (DIET) Electron transfer network Extended respiratory chain Geobacter Microbial fuel cell Shewanella 

References

  1. 1.
    Vargas M, Kashefi K, Blunt-Harris EL, Lovley DR (1998) Microbiological evidence for Fe(III) reduction on early earth. Nature 395:65–67PubMedGoogle Scholar
  2. 2.
    Prokhorova A, Sturm-Richter K, Doetsch A, Gescher J (2017) Resilience, dynamics and interactions within a multi-species exoelectrogenic model biofilm community. Appl Environ Microbiol 83(6):e03033–e03016PubMedPubMedCentralGoogle Scholar
  3. 3.
    Richter K, Schicklberger M, Gescher J (2012) Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl Environ Microbiol 78:913–921PubMedPubMedCentralGoogle Scholar
  4. 4.
    Sturm G, Dolch K, Richter K, Rautenberg M, Gescher J (2012) Metal reducers and reduction targets. A short survey about the distribution of dissimilatory metal reducers and the multitude of terminal electron acceptors. Microbial metal respiration: from geochemistry to potential applications. Springer-Verlag, Heidelberg, pp 129–159Google Scholar
  5. 5.
    Firer-Sherwood M, Pulcu GS, Elliott SJ (2008) Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window. J Biol Inorg Chem 13:849–854PubMedGoogle Scholar
  6. 6.
    Nevin KP, Lovley DR (2002) Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol J 19:141–159Google Scholar
  7. 7.
    Straub KL, Schink B (2003) Evaluation of electron-shuttling compounds in microbial ferric iron reduction. FEMS Microbiol Lett 220:229–233PubMedGoogle Scholar
  8. 8.
    Aklujkar M, Coppi MV, Leang C et al (2013) Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens. Microbiology 159:515–535PubMedGoogle Scholar
  9. 9.
    Butler JE, Young ND, Lovley DR (2010) Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 11:40PubMedPubMedCentralGoogle Scholar
  10. 10.
    Holmes DE, Chaudhuri SK, Nevin KP et al (2006) Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ Microbiol 8:1805–1815PubMedGoogle Scholar
  11. 11.
    Mehta T, Coppi MV, Childers SE, Lovley DR (2005) Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl Environ Microbiol 71:8634–8641PubMedPubMedCentralGoogle Scholar
  12. 12.
    Ding YHR, Hixson KK, Giometti CS et al (2006) The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions. Biochim Biophys Acta Proteins Proteomics 1764:1198–1206Google Scholar
  13. 13.
    Aklujkar M, Krushkal J, DiBartolo G, Lapidus A, Land ML, Lovley DR (2009) The genome sequence of Geobacter metallireducens: features of metabolism, physiology and regulation common and dissimilar to Geobacter sulfurreducens. BMC Microbiol 9(1):109PubMedPubMedCentralGoogle Scholar
  14. 14.
    Morgado L, Saraiva IH, Louro RO, Salgueiro CA (2010) Orientation of the axial ligands and magnetic properties of the hemes in the triheme ferricytochrome PpcA from G. sulfurreducens determined by paramagnetic NMR. FEBS Lett 584:3442–3445PubMedGoogle Scholar
  15. 15.
    Zacharoff L, Chan CH, Bond DR (2016) Reduction of low potential electron acceptors requires the CbcL inner membrane cytochrome of Geobacter sulfurreducens. Bioelectrochemistry 107:7–13PubMedGoogle Scholar
  16. 16.
    Levar CE, Chan CH, Mehta-Kolte MG, Bond DR (2014) An inner membrane cytochrome required only for reduction of high redox potential extracellular electron acceptors. MBio 5(6):e02034–e02014PubMedPubMedCentralGoogle Scholar
  17. 17.
    Seidel J, Hoffmann M, Ellis KE et al (2012) MacA is a second cytochrome c peroxidase of Geobacter sulfurreducens. Biochemistry 51:2747–2756PubMedPubMedCentralGoogle Scholar
  18. 18.
    Qian XL, Reguera G, Mester T, Lovley DR (2007) Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins. FEMS Microbiol Lett 277:21–27PubMedGoogle Scholar
  19. 19.
    Leang C, Coppi MV, Lovley DR (2003) OmcB, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J Bacteriol 185:2096–2103PubMedPubMedCentralGoogle Scholar
  20. 20.
    Liu X, Tremblay PL, Malvankar NS, Nevin KP, Lovley DR, Vargas M (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 80:1219–1224PubMedPubMedCentralGoogle Scholar
  21. 21.
    Liu YM, Fredrickson JK, Zachara JM, Shi L (2015) Direct involvement of ombB, omaB, and omcB genes in extracellular reduction of Fe(III) by Geobacter sulfurreducens PCA. Front Microbiol 6:–1075Google Scholar
  22. 22.
    Liu YM, Wang ZM, Liu J et al (2014) A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA. Environ Microbiol Rep 6:776–785PubMedPubMedCentralGoogle Scholar
  23. 23.
    Hartshorne RS, Reardon CL, Ross D et al (2009) Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci U S A 106:22169–22174PubMedPubMedCentralGoogle Scholar
  24. 24.
    Qian XL, Mester T, Morgado L et al (2011) Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens. BBA-Bioenergetics 1807:404–412PubMedGoogle Scholar
  25. 25.
    Leang C, Qian XL, Mester T, Lovley DR (2010) Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl Environ Microbiol 76:4080–4084PubMedPubMedCentralGoogle Scholar
  26. 26.
    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 330:1413–1415PubMedGoogle Scholar
  27. 27.
    Nevin KP, Kim BC, Glaven RH et al (2009) Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS One 4:e5628PubMedPubMedCentralGoogle Scholar
  28. 28.
    Strycharz SM, Glaven RH, Coppi MV et al (2011) Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemistry 80:142–150PubMedGoogle Scholar
  29. 29.
    Lovley DR (2011) Reach out and touch someone: potential impact of DIET (direct interspecies energy transfer) on anaerobic biogeochemistry, bioremediation, and bioenergy. Rev Environ Sci Biotechnol 10:101–105Google Scholar
  30. 30.
    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 80:4599–4605PubMedPubMedCentralGoogle Scholar
  31. 31.
    Rotaru AE, Shrestha PM, Liu FH 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. Energ Environ Sci 7:408–415Google Scholar
  32. 32.
    Rotaru AE, Shrestha PM, Liu FH, Ueki T, Nevin K, Summers ZM, Lovley DR (2012) Interspecies electron transfer via hydrogen and Formate rather than direct electrical connections in cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens. Appl Environ Microbiol 78:7645–7651PubMedPubMedCentralGoogle Scholar
  33. 33.
    Rollefson JB, Stephen CS, Tien M, Bond DR (2011) Identification of an extracellular polysaccharide network essential for cytochrome anchoring and biofilm formation in Geobacter sulfurreducens. J Bacteriol 193:1023–1033PubMedGoogle Scholar
  34. 34.
    Malvankar NS, Vargas M, Nevin KP et al (2011) Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol 6:573–579PubMedGoogle Scholar
  35. 35.
    Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101PubMedGoogle Scholar
  36. 36.
    Yates MD, Strycharz-Glaven SM, Golden JP, Roy J, Tsoi S, Erickson JS, El-Naggar MY, Barton SC, Tender LM (2016) Measuring conductivity of living Geobacter sulfurreducens biofilms. Nat Nanotechnol 11:910–913PubMedGoogle Scholar
  37. 37.
    Malvankar NS, Rotello VM, Tuominen MT, Lovley DR (2016) Reply to ‘Measuring conductivity of living Geobacter sulfurreducens biofilms’. Nat Nanotechnol 11:913–914PubMedGoogle Scholar
  38. 38.
    Childers SE, Ciufo S, Lovley DR (2002) Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416:767–769PubMedGoogle Scholar
  39. 39.
    Lovley DR (2012) Long-range electron transport to Fe(III) oxide via pili with metallic-like conductivity. Biochem Soc Trans 40:1186–1190PubMedGoogle Scholar
  40. 40.
    Malvankar NS, Tuominen MT, Lovley DR (2012) Lack of cytochrome involvement in long-range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens. Energ Environ Sci 5:8651–8659Google Scholar
  41. 41.
    Tremblay PL, Aklujkar M, Leang C, Nevin KP, Lovley D (2012) A genetic system for Geobacter metallireducens: role of the flagellin and pilin in the reduction of Fe(III) oxide. Environ Microbiol Rep 4:82–88PubMedGoogle Scholar
  42. 42.
    Shrestha PM, Rotaru AE, Aklujkar M et al (2013) Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. Environ Microbiol Rep 5:904–910PubMedGoogle Scholar
  43. 43.
    Vargas M, Malvankar NS, Tremblay PL et al (2013) Aromatic amino acids required for Pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. MBio 4(2):e00105–e00113PubMedPubMedCentralGoogle Scholar
  44. 44.
    Tan Y, Adhikari RY, Malvankar NS et al (2016) Synthetic biological protein nanowires with high conductivity. Small 12:4481–4485PubMedGoogle Scholar
  45. 45.
    Yi HN, Nevin KP, Kim BC, Franks AE, Klimes A, Tender LM, Lovley DR (2009) Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens Bioelectron 24:3498–3503PubMedGoogle Scholar
  46. 46.
    Burns JL, DiChristina TJ (2009) Anaerobic respiration of elemental sulfur and thiosulfate by Shewanella oneidensis MR-1 requires psrA, a homolog of the phsA gene of Salmonella enterica serovar Typhimurium LT2. Appl Environ Microbiol 75:5209–5217PubMedPubMedCentralGoogle Scholar
  47. 47.
    Gralnick JA, Vali H, Lies DP, Newman DK (2006) Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc Natl Acad Sci U S A 103:4669–4674PubMedPubMedCentralGoogle Scholar
  48. 48.
    Myers CR, Nealson KH (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron-acceptor. Science 240:1319–1321PubMedGoogle Scholar
  49. 49.
    Sturm G, Richter K, Doetsch A, Heide H, Louro RO, Gescher J (2015) A dynamic periplasmic electron transfer network enables respiratory flexibility beyond a thermodynamic regulatory regime. ISME J 9:1802–1811PubMedPubMedCentralGoogle Scholar
  50. 50.
    Myers CR, Myers JM (1997) Cloning and sequence of cymA a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J Bacteriol 179:1143–1152PubMedPubMedCentralGoogle Scholar
  51. 51.
    Beliaev AS, Klingeman DM, Klappenbach JA et al (2005) Global transcriptome analysis of Shewanella oneidensis MR-1 exposed to different terminal electron acceptors. J Bacteriol 187:7138–7145PubMedPubMedCentralGoogle Scholar
  52. 52.
    Schuetz B, Schicklberger M, Kuermann J, Spormann AM, Gescher J (2009) Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1. Appl Environ Microbiol 75:7789–7796PubMedPubMedCentralGoogle Scholar
  53. 53.
    McMillan DGG, Marritt SJ, Firer-Sherwood MA et al (2013) Protein-protein interaction regulates the direction of catalysis and electron transfer in a redox enzyme complex. J Am Chem Soc 135:10550–10556PubMedPubMedCentralGoogle Scholar
  54. 54.
    Alves MN, Neto SE, Alves AS et al (2015) Characterization of the periplasmic redox network that sustains the versatile anaerobic metabolism of Shewanella oneidensis MR-1. Front Microbiol 6:665.  https://doi.org/10.3389/fmicb.2015.00665 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Coursolle D, Baron DB, Bond DR, Gralnick JA (2010) The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. J Bacteriol 192:467–474PubMedGoogle Scholar
  56. 56.
    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 U S A 105:3968–3973PubMedPubMedCentralGoogle Scholar
  57. 57.
    von Canstein H, Ogawa J, Shimizu S, Lloyd JR (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74:615–623Google Scholar
  58. 58.
    Brutinel ED, Gralnick JA (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biotechnol 93:41–48PubMedGoogle Scholar
  59. 59.
    Baron D, LaBelle E, Coursolle D, Gralnick JA, Bond DR (2009) Electrochemical measurement of electron transfer kinetics by Shewanella oneidensis MR-1. J Biol Chem 284:28865–28873PubMedPubMedCentralGoogle Scholar
  60. 60.
    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(2):e16649PubMedPubMedCentralGoogle Scholar
  61. 61.
    Breuer M, Rosso KM, Blumberger J, Butt JN (2015) Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities. J R Soc Interface 12:20141117PubMedPubMedCentralGoogle Scholar
  62. 62.
    Clarke TA, Edwards MJ, Gates AJ et al (2011) Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci U S A 108:9384–9389PubMedPubMedCentralGoogle Scholar
  63. 63.
    Edwards MJ, White GF, Norman M et al (2015) Redox linked Flavin sites in extracellular Decaheme proteins involved in microbe-mineral electron transfer. Sci Rep 5:11677PubMedPubMedCentralGoogle Scholar
  64. 64.
    Okamoto A, Hashimoto K, Nealson KH, Nakamura R (2013) Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones. Proc Natl Acad Sci U S A 110:7856–7861PubMedPubMedCentralGoogle Scholar
  65. 65.
    Okamoto A, Nakamura R, Nealson KH, Hashimoto K (2014) Bound Flavin model suggests similar electron-transfer mechanisms in Shewanella and Geobacter. ChemElectroChem 1:1808–1812Google Scholar
  66. 66.
    Okamoto A, Kalathil S, Deng X, Hashimoto K, Nakamura R, Nealson KH (2014) Cell-secreted flavins bound to membrane cytochromes dictate electron transfer reactions to surfaces with diverse charge and pH. Sci Rep 4Google Scholar
  67. 67.
    Ding M, Shiu HY, Li SL et al (2016) Nanoelectronic investigation reveals the electrochemical basis of electrical conductivity in Shewanella and Geobacter. ACS Nano 10:9919–9926PubMedGoogle Scholar
  68. 68.
    Koch C, Harnisch F (2016) Is there a specific ecological niche for electroactive microorganisms? ChemElectroChem 3:1282–1295Google Scholar
  69. 69.
    Carlson HK, Iavarone AT, Gorur A et al (2012) Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram- positive bacteria. Proc Natl Acad Sci U S A 109:1702–1707PubMedPubMedCentralGoogle Scholar
  70. 70.
    Wrighton KC, Thrash JC, Melnyk RA et al (2011) Evidence for direct electron transfer by a Gram-positive bacterium isolated from a microbial fuel cell. Appl Environ Microbiol 77:7633–7639PubMedPubMedCentralGoogle Scholar
  71. 71.
    Lusk BG, Parameswaran P, Popat SC, Rittmann BE, Torres CI (2016) The effect of pH and buffer concentration on anode biofilms of Thermincola ferriacetica. Bioelectrochemistry 112:47–52PubMedGoogle Scholar
  72. 72.
    Clark Jr LC, Lyons C (1962) Electrode systems for continuous monitoring un cardiovascular surgery. Ann N Y Acad Sci 102:29–45PubMedGoogle Scholar
  73. 73.
    Setford SJ, Newman JD (2005) Enzyme biosensors. vol 17, pp 29–60Google Scholar
  74. 74.
    Turner AP, Karube I, Wilson GS (1987) Biosensors fundamentals and applications. Oxford Science Publications, Oxford, EngalndGoogle Scholar
  75. 75.
    Lazcka O, Del Campo FJ, Munoz FX (2007) Pathogen detection: a perspective of traditional methods and biosensors. Biosens Bioelectron 22:1205–1217PubMedGoogle Scholar
  76. 76.
    Luong JH, Male KB, Glennon JD (2008) Biosensor technology: technology push versus market pull. Biotechnol Adv 26:492–500PubMedGoogle Scholar
  77. 77.
    Su L, Jia W, Hou C, Lei Y (2011) Microbial biosensors: a review. Biosens Bioelectron 26:1788–1799PubMedGoogle Scholar
  78. 78.
    Belkin S (2003) Microbial whole-cell sensing systems of environmental pollutants. Curr Opin Microbiol 6:206–212PubMedGoogle Scholar
  79. 79.
    Kumlanghan A, Kanatharana P, Asawatreratanakul P, Mattiasson B, Thavarungkul P (2008) Microbial BOD sensor for monitoring treatment of wastewater from a rubber latex industry. Enzyme Microb Technol 42:483–491Google Scholar
  80. 80.
    Nakamura H, Suzuki K, Ishikuro H et al (2007) A new BOD estimation method employing a double-mediator system by ferricyanide and menadione using the eukaryote Saccharomyces cerevisiae. Talanta 72:210–216PubMedGoogle Scholar
  81. 81.
    APHA (1998) Standard methods for the examination of waters and wastewaters, vol 20. American Public Health Association, WashingtonGoogle Scholar
  82. 82.
    SIS (1979) Water analysis - determination of biochemical oxygen demand, BOD, of water dilution method (Svensk standard SS 02 81 43 E), vol 1. The Swedish Standards Institution, StockholmGoogle Scholar
  83. 83.
    Chang IS, Jang JK, Gil GC, Kim M, Kim HJ, Cho BW, Kim BH (2004) Continuous determination of biochemical oxygen demand using microbial fuel cell type biosensor. Biosens Bioelectron 19:607–613PubMedGoogle Scholar
  84. 84.
    Kim BH, Chang IS, Gil GC, Park HS, Kim HJ (2003) Novel BOD (biochemical oxygen demand) sensor using mediator-less microbial fuel cell. Biotechnol Lett 25:541–545PubMedGoogle Scholar
  85. 85.
    Clark Jr LC (1956) Monitor and control of blood and tissue oxygen tensions. Trans Am Soc Artif Intern Organs 2(1):41–48Google Scholar
  86. 86.
    Karube I, Matsunaga T, Mitsuda S, Suzuki S (1977) Microbial electrode BOD sensors. Biotechnol Bioeng XIX:1535–1547Google Scholar
  87. 87.
    Liu J, Mattiasson B (2002) Microbial BOD sensors for wastewater analysis. Water Res 36:3786–3802PubMedGoogle Scholar
  88. 88.
    Ponomareva ON, Arlyapov VA, Alferov VA, Reshetilov AN (2011) Microbial biosensors for detection of biological oxygen demand (a review). Appl Biochem Microbiol 47:1–11Google Scholar
  89. 89.
    Liu J, Bjornsson L, Mattiasson B (2000) Immobilised activated sludge based biosensor for biochemical oxygen demand measurement. Biosens Bioelectron 14(12):883–893PubMedGoogle Scholar
  90. 90.
    Chee G, Nomura Y, Karube I (1999) Biosensor for the estimation of low biochemical oxygen demand. Anal Chim Acta 379:185–191Google Scholar
  91. 91.
    Kulys J, Kadziauskiene K (1980) Yeast BOD sensor. Biotechnol Bioeng XXII:221–226Google Scholar
  92. 92.
    Marty JL, Olive D, Asano Y (1997) Measurement of BOD: correlation between 5-day BOD and commercial BOD biosensor values. Environ Technol 18:333–337Google Scholar
  93. 93.
    Riedel K, Renneberg R, Kühn M, Scheller F (1988) A fast estimation of biochemical oxygen demandusing microbial sensors. Appl Microbiol Biotechnol 28:316–318Google Scholar
  94. 94.
    Kang KH, Jang JK, Pham TH, Moon H, Chang IS, Kim BH (2003) A microbial fuel cell with improved cathode reaction as a low biochemical oxygen demand sensor. Biotechnol Lett 25:1357–1361PubMedGoogle Scholar
  95. 95.
    Grzebyk M, Poźniak G (2005) Microbial fuel cells (MFCs) with interpolymer cation exchange membranes. Sep Purif Technol 41:321–328Google Scholar
  96. 96.
    Rabaey K, Verstraete W (2005) Microbial fuel cells: novel biotechnology for energy generation. Trends Biotechnol 23:291–298PubMedGoogle Scholar
  97. 97.
    Tkac J, Vostiar I, Gorton L, Gemeiner P, Sturdik E (2003) Improved selectivity of microbial biosensor using membrane coating. Application to the analysis of ethanol during fermentation. Biosens Bioelectron 18:1125–1134PubMedGoogle Scholar
  98. 98.
    Trosok SP, Driscoll BT, Luong JHT (2001) Mediated microbial biosensor using a novel yeast strain for wastewater BOD measurement. Appl Microbiol Biotechnol 56:550–554PubMedGoogle Scholar
  99. 99.
    Yoshida N, Hoashi J, Morita T, McNiven S, Nakamura H, Karube I (2001) Improvement of a mediator-type biochemical oxygen demand sensor for on-site measurement. J Biotechnol 88:269–275PubMedGoogle Scholar
  100. 100.
    Pasco NF, Baronian K, Jeffries C, Hay J (2000) Biochemical mediator demand - a novel rapid alternative for measuring biochemical oxygen demand. Appl Microbiol Biotechnol 53:613–618PubMedGoogle Scholar
  101. 101.
    Morris K, Zhao H, John R (2003) The use of a mixed microbial consortium in a rapid ferricyanide mediated biochemical oxygen demand assay. Trans Ecol Environ:65Google Scholar
  102. 102.
    Gil G-C, Chang I-S, Kim BH, Kim M, Jang J-K, Park HS, Kim HJ (2003) Operational parameters affecting the performannce of a mediator-less microbial fuel cell. Biosens Bioelectron 18:327–334PubMedGoogle Scholar
  103. 103.
    Pasco NF, Weld RJ, Hay JM, Gooneratne R (2011) Development and applications of whole cell biosensors for ecotoxicity testing. Anal Bioanal Chem 400:931–945PubMedGoogle Scholar
  104. 104.
    Kumlanghan A, Liu J, Thavarungkul P, Kanatharana P, Mattiasson B (2007) Microbial fuel cell-based biosensor for fast analysis of biodegradable organic matter. Biosens Bioelectron 22:2939–2944PubMedGoogle Scholar
  105. 105.
    Di Lorenzo M, Curtis TP, Head IM, Scott K (2009) A single-chamber microbial fuel cell as a biosensor for wastewaters. Water Res 43:3145–3154PubMedGoogle Scholar
  106. 106.
    Di Lorenzo M, Thomson AR, Schneider K, Cameron PJ, Ieropoulos I (2014) A small-scale air-cathode microbial fuel cell for on-line monitoring of water quality. Biosens Bioelectron 62:182–188PubMedGoogle Scholar
  107. 107.
    Kim M, Sik Hyun M, Gadd GM, Joo Kim H (2007) A novel biomonitoring system using microbial fuel cells. J Environ Monit 9:1323–1328PubMedGoogle Scholar
  108. 108.
    Stein NE, Hamelers HMV, van Straten G, Keesman KJ (2012) On-line detection of toxic components using a microbial fuel cell-based biosensor. J Process Control 22:1755–1761Google Scholar
  109. 109.
    Wang B, Barahona M, Buck M (2013) A modular cell-based biosensor using engineered genetic logic circuits to detect and integrate multiple environmental signals. Biosens Bioelectron 40:368–376PubMedPubMedCentralGoogle Scholar
  110. 110.
    Hernandez Leal L, Soeter AM, Kools SA et al (2012) Ecotoxicological assessment of grey water treatment systems with Daphnia magna and Chironomus riparius. Water Res 46:1038–1044PubMedGoogle Scholar
  111. 111.
    Matsunaga T, Takeyama H, Nakao T, Yamazawa A (1999) Screening of marine microalgae for bioremediation of cadmium- polluted seawater. J Biotechnol 70:33–38PubMedGoogle Scholar
  112. 112.
    Qu R, Wang X, Liu Z, Yan Z, Wang Z (2013) Development of a model to predict the effect of water chemistry on the acute toxicity of cadmium to Photobacterium phosphoreum. J Hazard Mater 262:288–296PubMedGoogle Scholar
  113. 113.
    Zhang H, Cao H, Meng Y, Jin G, Zhu M (2012) The toxicity of cadmium (Cd(2)(+)) towards embryos and pro-larva of soldatov’s catfish (Silurus Soldatovi). Ecotoxicol Environ Saf 80:258–265PubMedGoogle Scholar
  114. 114.
    Lee H, Yang W, Wei X, Fraiwan A, Choi S (2015) A microsized microbial fuel cell based biosensor for fast and sensitive detection of toxic substances in waterGoogle Scholar
  115. 115.
    Patil S, Harnisch F, Schroder U (2010) Toxicity response of electroactive microbial biofilms - a decisive feature for potential biosensor and power source applications. ChemPhysChem 11:2834–2837PubMedGoogle Scholar
  116. 116.
    Davila D, Esquivel JP, Sabate N, Mas J (2011) Silicon-based microfabricated microbial fuel cell toxicity sensor. Biosens Bioelectron 26:2426–2430PubMedGoogle Scholar
  117. 117.
    Tront JM, Fortner JD, Plotze M, Hughes JB, Puzrin AM (2008) Microbial fuel cell biosensor for in situ assessment of microbial activity. Biosens Bioelectron 24:586–590PubMedGoogle Scholar
  118. 118.
    Tront JM, Fortner JD, Plotze M, Hughes JB, Puzrin AM (2008) Microbial fuel cell technology for measurement of microbial respiration of lactate as an example of bioremediation amendment. Biotechnol Lett 30:1385–1390PubMedGoogle Scholar
  119. 119.
    Holtmann D, Sell D (2002) Detection of the microbial activity of aerobic heterotrophic, anoxic heterotrophic and aerobic autotrophic activated sludge organisms with an electrochemical sensor. Biotechnol Lett 24:1313–1318Google Scholar
  120. 120.
    Holtmann D, Schrader J, Sell D (2006) Quantitative comparison of the signals of an electrochemical bioactivity sensor during the cultivation of different microorganisms. Biotechnol Lett 28:889–896PubMedGoogle Scholar
  121. 121.
    Golitsch F, Bücking C, Gescher J (2013) Proof of principle for an engineered microbial biosensor based on Shewanella oneidensis outer membrane protein complexes. Biosens Bioelectron 47:285–291PubMedGoogle Scholar
  122. 122.
    Bücking C, Popp F, Kerzenmacher S, Gescher J (2010) Involvement and specificity of Shewanella oneidensis outer membrane cytochromes in the reduction of soluble and solid-phase terminal electron acceptors. FEMS Microbiol Lett 306:144–151PubMedGoogle Scholar
  123. 123.
    Webster DP, TerAvest MA, Doud DF et al (2014) An arsenic-specific biosensor with genetically engineered Shewanella oneidensis in a bioelectrochemical system. Biosens Bioelectron 62:320–324PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Francesca Simonte
    • 1
  • Gunnar Sturm
    • 1
  • Johannes Gescher
    • 1
    • 2
  • Katrin Sturm-Richter
    • 1
    Email author
  1. 1.Department of Applied BiologyInstitute for Applied Biosciences, Karlsruhe Institute of TechnologyKarlsruheGermany
  2. 2.Department of Microbiology of Natural and Technical InterfacesInstitute of Functional Interfaces, Karlsruhe Institute of TechnologyEggenstein-LeopoldshafenGermany

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