On-going applications of Shewanella species in microbial electrochemical system for bioenergy, bioremediation and biosensing

  • Long Zou
  • Yun-hong Huang
  • Zhong-er LongEmail author
  • Yan QiaoEmail author


Microbial electrochemical system (MES) has attracted ever-growing interest as a promising platform for renewable energy conversion and bioelectrochemical remediation. Shewanella species, the dissimilatory metal reduction model bacteria with versatile extracellular electron transfer (EET) strategies, are the well-received microorganisms in diverse MES devices for various practical applications as well as microbial EET mechanism investigation. Meanwhile, the available genomic information and the unceasing established gene-editing toolbox offer an unprecedented opportunity to boost the applications of Shewanella species in MES. This review thoroughly summarizes the status quo of the applications of Shewanella species in microbial fuel cells for bioelectricity generation, microbial electrosynthesis for biotransformation of valuable chemicals and bioremediation of environment-hazardous pollutants with synoptical discussion on their EET mechanism. Recent advances in rational design and genetic engineering of Shewanella strains for either promoting the MES performance or broadening their applications are surveyed. Moreover, some emerging applications beyond electricity generation, such as biosensing and biocomputing, are also documented. The challenges and perspectives for Shewanella-based MES are also discussed elaborately for the sake of not only discovering new scientific lights on microbial extracellular respiratory but also propelling practical applications.

Graphical abstract


Shewanella Extracellular electron transfer Microbial fuel cell Microbial electrosynthesis Bioelectrochemical remediation Biosensing 



This work was financially supported by the Natural Science Foundation of Jiangxi Province (No. 20181BAB213004), the Fundamental Research Funds for the Central Universities (No. XDJK2018B003) and the Sponsored Program for Cultivating Youths of Outstanding Ability in Jiangxi Normal University.


  1. Abrevaya XC, Sacco NJ, Bonetto MC et al (2015) Analytical applications of microbial fuel cells. Part II: toxicity, microbial activity and quantification, single analyte detection and other uses. Biosens Bioelectron 63:591–601PubMedGoogle Scholar
  2. Babu SS, Mohandass C, Raj ASV et al (2013) Multiple approaches towards decolorization and reuse of a textile dye (VB-B) by a marine bacterium Shewanella decolorationis. Water Air Soil Poll 224:1500Google Scholar
  3. Bretschger O, Cheung ACM, Mansfeld F, Nealson KH (2010) Comparative microbial fuel cell evaluations of Shewanella spp. Electroanalysis 22:883–894Google Scholar
  4. Brutinel ED, Gralnick JA (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biotechnol 93:41–48PubMedGoogle Scholar
  5. Cao DM, Xiao X, Wu YM et al (2013) Role of electricity production in the anaerobic decolorization of dye mixture by exoelectrogenic bacterium Shewanella oneidensis MR-1. Bioresource Technol 136:176–181Google Scholar
  6. Cao Y, Li X, Li F, Song H (2017) CRISPRi–sRNA: transcriptional-translational regulation of extracellular electron transfer in Shewanella oneidensis. ACS Synth Biol 6:1679–1690PubMedGoogle Scholar
  7. 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
  8. Ding C-m, Lv M-l, Zhu Y et al (2015) Wettability-regulated extracellular electron transfer from the living organism of Shewanella loihica PV-4. Angew Chem Int Ed 54:1446–1451Google Scholar
  9. Drewniak L, Stasiuk R, Uhrynowski W, Sklodowska A (2015) Shewanella sp O23S as a driving agent of a system utilizing dissimilatory arsenate-reducing bacteria responsible for self-cleaning of water contaminated with arsenic. Int J Mol Sci 16:14409–14427PubMedPubMedCentralGoogle Scholar
  10. Fernando E, Keshavarz T, Kyazze G (2012) Enhanced bio-decolourisation of acid orange 7 by Shewanella oneidensis through co-metabolism in a microbial fuel cell. Int Biodeterior Biodegrad 72:1–9Google Scholar
  11. Gao S-H, Peng L, Liu Y et al (2016a) Bioelectrochemical reduction of an azo dye by a Shewanella oneidensis MR-1 formed biocathode. Int Biodeterior Biodegrad 115:250–256Google Scholar
  12. Gao SH, Peng L, Liu YW et al (2016b) Bioelectrochemical reduction of an azo dye by a Shewanella oneidensis MR-1 formed biocathode. Int Biodeterior Biodegrad 115:250–256Google Scholar
  13. 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
  14. Gomaa OM, Fapetu S, Kyazze G, Keshavarz T (2017) The role of riboflavin in decolourisation of Congo red and bioelectricity production using Shewanella oneidensis MR-1 under MFC and non-MFC conditions. World J Microbiol Biotechnol 33:56PubMedGoogle Scholar
  15. Han K, Yueh P-L, Qin L-J et al (2015) Deciphering synergistic characteristics of microbial fuel cell-assisted dye decolorization. Bioresour Technol 196:746–751PubMedGoogle Scholar
  16. Han JC, Chen GJ, Qin LP, Mu Y (2017) Metal respiratory pathway-independent Cr isotope fractionation during Cr(VI) reduction by Shewanella oneidensis MR-1. Environ Sci Technol Lett 4:500–504Google Scholar
  17. Hu Y, Yang Y, Katz E, Song H (2015) Programming the quorum sensing-based AND gate in Shewanella oneidensis for logic gated-microbial fuel cells. Chem Commun 51:4184–4187Google Scholar
  18. Imran M, Arshad M, Asghar HN et al (2014) Potential of Shewanella sp strain IFN4 to decolorize azo dyes under optimal conditions. Int J Agric Biol 16:578–584Google Scholar
  19. Jeon J-M, Park H, Seo H-M et al (2015) Isobutanol production from an engineered Shewanella oneidensis MR-1. Bioprocess Biosyst Eng 38:2147–2154PubMedGoogle Scholar
  20. Jiang S, Cuong Tu H, Lee J-H et al (2012) Mercury capture into biogenic amorphous selenium nanospheres produced by mercury resistant Shewanella putrefaciens 200. Chemosphere 87:621–624PubMedGoogle Scholar
  21. Jorge AB, Hazael R (2016) Use of Shewanella oneidensis for energy conversion in microbial fuel cells. Macromol Chem Phys 217:1431–1438Google Scholar
  22. Kim BH, Ikeda T, Park HS et al (1999) Electrochemical activity of an Fe(III)-reducing bacterium, Shewanella putrefaciens IR-1, in the presence of alternative electron acceptors. Biotechnol Tech 13:475–478Google Scholar
  23. Kumar R, Singh L, Zularisam A (2016) Exoelectrogens: recent advances in molecular drivers involved in extracellular electron transfer and strategies used to improve it for microbial fuel cell applications. Renew Sustain Energy Rev 56:1322–1336Google Scholar
  24. Kumar A, Hsu LH-H, Kavanagh P et al (2017) The ins and outs of microorganism-electrode electron transfer reactions. Nat Rev Chem 1:0024Google Scholar
  25. La JA, Jeon J-M, Sang B-I et al (2017) A hierarchically modified graphite cathode with Au nanoislands, cysteamine, and Au nanocolloids for increased electricity-assisted production of isobutanol by engineered Shewanella oneidensis MR-1. ACS Appl Mater Interfaces 9:43563–43574PubMedGoogle Scholar
  26. Le QAT, Kim HG, Kim YH (2018) Electrochemical synthesis of formic acid from CO2 catalyzed by Shewanella oneidensis MR-1 whole-cell biocatalyst. Enzym Microb Technol 116:1–5Google Scholar
  27. Li SL, Freguia S, Liu SM et al (2010) Effects of oxygen on Shewanella decolorationis NTOU1 electron transfer to carbon-felt electrodes. Biosens Bioelectron 25:2651–2656PubMedGoogle Scholar
  28. Li Z, Rosenbaum MA, Venkataraman A et al (2011) Bacteria-based AND logic gate: a decision-making and self-powered biosensor. Chem Commun 47:3060–3062Google Scholar
  29. Li F, Li Y, Sun L et al (2017a) Engineering Shewanella oneidensis enables xylose-fed microbial fuel cell. Biotechnol Biofuels 10:196PubMedPubMedCentralGoogle Scholar
  30. Li S-W, Zeng RJ, Sheng G-P (2017b) An excellent anaerobic respiration mode for chitin degradation by Shewanella oneidensis MR-1 in microbial fuel cells. Biochem Eng J 118:20–24Google Scholar
  31. Li F, Li Y-X, Cao Y-X et al (2018a) Modular engineering to increase intracellular NAD(H/+) promotes rate of extracellular electron transfer of Shewanella oneidensis. Nat Commun 9:3637PubMedPubMedCentralGoogle Scholar
  32. Li F, Li Y, Sun L et al (2018b) Modular engineering intracellular NADH regeneration boosts extracellular electron transfer of Shewanella oneidensis MR-1. ACS Synth Biol 7:885–895PubMedGoogle Scholar
  33. Li Q, Feng X-L, Li T-T et al (2018c) Anaerobic decolorization and detoxification of cationic red X-GRL by Shewanella oneidensis MR-1. Environ Technol 39:2382–2389PubMedGoogle Scholar
  34. Liu T, Yu YY, Deng XP et al (2015) Enhanced Shewanella biofilm promotes bioelectricity generation. Biotechnol Bioeng 112:2051–2059PubMedGoogle Scholar
  35. Liu TX, Li XM, Li FB et al (2016) In situ spectral kinetics of Cr(VI) reduction by c-type cytochromes in a suspension of living Shewanella putrefaciens 200. Sci Rep 6:29592PubMedPubMedCentralGoogle Scholar
  36. Liu X, Shi L, Gu J-D (2018) Microbial electrocatalysis: redox mediators responsible for extracellular electron transfer. Biotechnol Adv 36:1815–1827PubMedGoogle Scholar
  37. Logan BE, Rabaey K (2012) Conversion of wastes into bioelectricity and chemicals by using microbial electrochemical technologies. Science 337:686–690PubMedGoogle Scholar
  38. Mao F, Liu XH, Wu K et al (2018) Biodegradation of sulfonamides by Shewanella oneidensis MR-1 and Shewanella sp strain MR-4. Biodegradation 29:129–140PubMedGoogle Scholar
  39. Min D, Cheng L, Zhang F et al (2017) Enhancing extracellular electron transfer of Shewanella oneidensis MR-1 through coupling improved flavin synthesis and metal-reducing conduit for pollutant degradation. Environ Sci Technol 51:5082–5089PubMedGoogle Scholar
  40. Newton GJ, Mori S, Nakamura R et al (2009) Analyses of current-generating mechanisms of Shewanella loihica PV-4 and Shewanella oneidensis MR-1 in microbial fuel cells. Appl Environ Microbiol 75:7674–7681PubMedPubMedCentralGoogle Scholar
  41. Ng IS, Chen TT, Lin R et al (2014) Decolorization of textile azo dye and Congo red by an isolated strain of the dissimilatory manganese-reducing bacterium Shewanella xiamenensis BC01. Appl Microbiol Biotechnol 98:2297–2308PubMedGoogle Scholar
  42. Ogi T, Tamaoki K, Saitoh N et al (2012) Recovery of indium from aqueous solutions by the Gram-negative bacterium Shewanella algae. Biochem Eng J 63:129–133Google Scholar
  43. Okamoto A, Hashimoto K, Nealson KH, Nakamura R (2013) Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones. Proc Natl Acad Sci USA 110:7856–7861PubMedGoogle Scholar
  44. Pirbadian S, Barchinger SE, Leung KM et al (2014) Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc Natl Acad Sci USA 111:12883–12888PubMedGoogle Scholar
  45. Prevoteau A, Rabaey K (2017) Electroactive biofilms for sensing: reflections and perspectives. ACS Sens 2:1072–1085PubMedGoogle Scholar
  46. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis-revisiting the electrical route for microbial production. Nat Rev Microbiol 8:706–716PubMedGoogle Scholar
  47. Riccobono G, Pastorella G, Vicari F et al (2017) Abatement of AO7 in a divided microbial fuel cells by sequential cathodic and anodic treatment powered by different microorganisms. J Electroanal Chem 799:293–298Google Scholar
  48. Ross DE, Flynn JM, Baron DB et al (2011) Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism. PLoS ONE 6:e16649PubMedPubMedCentralGoogle Scholar
  49. Santoro C, Arbizzani C, Erable B, Ieropoulos I (2017) Microbial fuel cells: from fundamentals to applications. A review. J Power Sources 356:225–244PubMedPubMedCentralGoogle Scholar
  50. Shin HJ, Jung KA, Nam CW, Park JM (2017) A genetic approach for microbial electrosynthesis system as biocommodities production platform. Bioresour Technol 245:1421–1429PubMedGoogle Scholar
  51. Si R-W, Zhai D-D, Liao Z-H et al (2015) A whole-cell electrochemical biosensing system based on bacterial inward electron flow for fumarate quantification. Biosens Bioelectron 68:34–40PubMedGoogle Scholar
  52. Si RW, Yang Y, Yu YY et al (2016) Wiring bacterial electron flow for sensitive whole-cell amperometric detection of riboflavin. Anal Chem 88:11222–11228PubMedGoogle Scholar
  53. Szczuka A, Morel FMM, Schaefer JK (2015) Effect of thiols, zinc, and redox conditions on Hg uptake in Shewanella oneidensis. Environ Sci Technol 49:7432–7438PubMedGoogle Scholar
  54. Tao L, Xie M, Chiew GGY et al (2016) Improving electron trans-inner membrane movements in microbial electrocatalysts. Chem Commun 52:6292–6295Google Scholar
  55. TerAvest MA, Li ZJ, Angenent LT (2011) Bacteria-based biocomputing with cellular computing circuits to sense, decide, signal, and act. Energy Environ Sci 4:4907–4916Google Scholar
  56. Ueki T, Nevin KP, Woodard TL, Lovley DR (2016) Genetic switches and related tools for controlling gene expression and electrical outputs of Geobacter sulfurreducens. J Ind Microbiol Biotechnol 43:1561–1575PubMedGoogle Scholar
  57. Vikrant K, Giri BS, Raza N et al (2018) Recent advancements in bioremediation of dye: current status and challenges. Bioresource Technol 253:355–367Google Scholar
  58. Wang J, Lu H, Zhou Y et al (2013a) Enhanced biotransformation of nitrobenzene by the synergies of Shewanella species and mediator-functionalized polyurethane foam. J Hazard Mater 252:227–232PubMedGoogle Scholar
  59. Wang X, Gao N, Zhou Q (2013b) Concentration responses of toxicity sensor with Shewanella oneidensis MR-1 growing in bioelectrochemical systems. Biosens Bioelectron 43:264–267PubMedGoogle Scholar
  60. Wang H, Luo H, Fallgren PH et al (2015) Bioelectrochemical system platform for sustainable environmental remediation and energy generation. Biotechnol Adv 33:317–334PubMedGoogle Scholar
  61. Wang GY, Zhang BG, Li S et al (2017a) Simultaneous microbial reduction of vanadium(V) and chromium(VI) by Shewanella loihica PV-4. Bioresour Technol 227:353–358PubMedGoogle Scholar
  62. Wang Y-Z, Shen Y, Gao L et al (2017b) Improving the extracellular electron transfer of Shewanella oneidensis MR-1 for enhanced bioelectricity production from biomass hydrolysate. RSC Adv 7:30488–30494Google Scholar
  63. Wang W, Zhang BG, Liu QS et al (2018) Biosynthesis of palladium nanoparticles using Shewanella loihica PV-4 for excellent catalytic reduction of chromium(VI). Environ Sci Nano 5:730–739Google Scholar
  64. Webster DP, TerAvest MA, Doud DFR et al (2014) An arsenic-specific biosensor with genetically engineered Shewanella oneidensis in a bioelectrochemical system. Biosens Bioelectron 62:320–324PubMedGoogle Scholar
  65. West EA, Jain A, Gralnick JA (2017) Engineering a native inducible expression system in Shewanella oneidensis to control extracellular electron transfer. ACS Synth Biol 6:1627–1634PubMedGoogle Scholar
  66. Wu WG, Yang F, Liu X, Bai LL (2014) Influence of substrate on electricity generation of Shewanella loihica PV-4 in microbial fuel cells. Microb Cell Fact 13:69PubMedPubMedCentralGoogle Scholar
  67. Wu X, Zou L, Huang Y et al (2018) Shewanella putrefaciens CN32 outer membrane cytochromes MtrC and UndA reduce electron shuttles to produce electricity in microbial fuel cells. Enzym Microb Technol 115:23–28Google Scholar
  68. Xafenias N, Zhang Y, Banks CJ (2015) Evaluating hexavalent chromium reduction and electricity production in microbial fuel cells with alkaline cathodes. Int J Environ Sci Technol 12:2435–2446Google Scholar
  69. Yang Y, Xu M, Guo J, Sun G (2012) Bacterial extracellular electron transfer in bioelectrochemical systems. Process Biochem 47:1707–1714Google Scholar
  70. Yang Y, Ding Y, Hu Y et al (2015) Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway. ACS Synth Biol 4:815–823PubMedGoogle Scholar
  71. Yang Y, Liu T, Zhu X et al (2016) Boosting power density of microbial fuel cells with 3D nitrogen-doped graphene aerogel electrode. Adv Sci 3:1600097Google Scholar
  72. Yang Y, Kong G, Chen X et al (2017a) Electricity generation by Shewanella decolorationis S12 without cytochrome c. Front Microbiol 8:115Google Scholar
  73. Yang Y, Yu YY, Wang YZ et al (2017b) Amplification of electrochemical signal by a whole-cell redox reactivation module for ultrasensitive detection of pyocyanin. Biosens Bioelectron 98:338–344PubMedGoogle Scholar
  74. Yang Y, Wang YZ, Fang Z et al (2018) Bioelectrochemical biosensor for water toxicity detection: generation of dual signals for electrochemical assay confirmation. Anal Bioanal Chem 410:1231–1236PubMedGoogle Scholar
  75. Yi Y, Xie BZ, Zhao T, Liu H (2018) Comparative analysis of microbial fuel cell based biosensors developed with a mixed culture and Shewanella loihica PV-4 and underlying biological mechanism. Bioresour Technol 265:415–421PubMedGoogle Scholar
  76. Zhang HK, Lu H, Wang J et al (2014) Accelerating effect of bio-reduced graphene oxide on decolorization of Acid Red 18 by Shewanella algae. Appl Biochem Biotechnol 174:602–611PubMedGoogle Scholar
  77. Zhang C-L, Yu Y-Y, Fang Z et al (2018) Recent advances in nitroaromatic pollutants bioreduction by electroactive bacteria. Process Biochem 70:129–135Google Scholar
  78. Zhou Y, Lu H, Wang J et al (2018) Catalytic performance of quinone and graphene-modified polyurethane foam on the decolorization of azo dye Acid Red 18 by Shewanella sp RQs-106. J Hazard Mater 356:82–90PubMedGoogle Scholar
  79. Zhu G, Yang Y, Liu J et al (2017) Enhanced photocurrent production by the synergy of hematite nanowire-arrayed photoanode and bioengineered Shewanella oneidensis MR-1. Biosens Bioelectron 94:227–234PubMedGoogle Scholar
  80. Zou L, Qiao Y, Wu X-S, Li CM (2016a) Tailoring hierarchically porous graphene architecture by carbon nanotube to accelerate extracellular electron transfer of anodic biofilm in microbial fuel cells. J Power Sources 328:143–150Google Scholar
  81. Zou L, Qiao Y, Wu Z-Y et al (2016b) Tailoring unique mesopores of hierarchically porous structures for fast direct electrochemistry in microbial fuel cells. Adv Energy Mater 6:1501535Google Scholar
  82. Zou L, Lu Z, Huang Y et al (2017a) Nanoporous Mo2C functionalized 3D carbon architecture anode for boosting flavins mediated interfacial bioelectrocatalysis in microbial fuel cells. J Power Sources 359:549–555Google Scholar
  83. Zou L, Qiao Y, Zhong C, Li CM (2017b) Enabling fast electron transfer through both bacterial outer-membrane redox centers and endogenous electron mediators by polyaniline hybridized large-mesoporous carbon anode for high-performance microbial fuel cells. Electrochim Acta 229:31–38Google Scholar
  84. Zou L, Qiao Y, Li CM (2018) Boosting microbial electrocatalytic kinetics for high power density: insights into synthetic biology and advanced nanoscience. Electrochem Energy Rev 1:567–596Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.College of Life SciencesJiangxi Normal UniversityNanchangChina
  2. 2.Institute for Clean Energy and Advanced Materials, Faculty of Materials and EnergySouthwest UniversityChongqingChina

Personalised recommendations