350 rub
Journal Technologies of Living Systems №4 for 2022 г.
Article in number:
Prospects for the use of electroactive microorganisms for the production of environmentally friendly energy
Type of article: overview article
DOI: https://doi.org/10.18127/j20700997-202204-07
UDC: 579.66
Authors:

E.R. Faskhutdinova1, M.Yu. Drozdova2, A.I. Dmitrieva3

1–3 Kemerovo State University (Kemerovo, Russia)

Abstract:

The active use of oil, gas and coal causes irreparable damage to the environment. A new and promising solution to this problem is the technology of a microbial fuel cell, which allows converting chemical energy into electrical energy. The key role in this system belongs to microorganisms with electroactive properties. The purpose of this review is to study the electroactive properties of various groups of microorganisms to obtain environmentally friendly energy.

Among the electroactive microorganisms, bacteria, fungi, yeast and microalgae are isolated. The most common electroactive microorganisms are Shewanella and Geobacter bacteria due to the ability to generate a significant amount of energy, the annotated sequence of the Shewanella genome and the ability of Geobacter to participate in bioremediation. Pseudomonas aeruginosa and Escherichia coli generate a relatively low amount of energy, besides their electroactive ability is due to genetic manipulation. Electroactive microorganisms are also representatives of yeast (Candida fukuyamaensis, Lipomyces starkeyi and Saccharomyces cerevisiae) and white rot fungi (Ganoderma lucidum, Pleurotus eryngii, Simplicillium oblavatum). Promising electroactive microorganisms are microalgae. They are able to synthesize energy in light conditions. Microalgae such as Chlorella sp have found their application in microbial fuel cell technology.

During the scientific review, it was found that electroactive microorganisms are present in many groups of microorganisms. Understanding their diversity and unique electronic capabilities leads to a wide range of applications, for example, the removal of heavy metals and azo dyes from wastewater, polycyclic aromatic hydrocarbons from wastewater, as well as salt water desalination.

Pages: 70-82
For citation

Faskhutdinova E.R., Drozdova M.Yu., Dmitrieva A.I. Prospects for the use of electroactive microorganisms for the production of environmentally friendly energy. Technologies of Living Systems. 2022. V. 19. № 4. Р. 70-82. DOI: https://doi.org/10.18127/j20700997-202204-07 (In Russian)

References
  1. Tyurin-Kuzmin A.Yu., Korshunov D.V., Punegova A.V., Suprunova Yu.V., Dubovitskaya V.A., Smirnov I.A., Ilin V.K. Mikrobnyy toplivnyy element kak model flokkuly – strukturno-funktsionalnoy edinitsy aktivnogo ila. Tekhnologii zhivykh sistem. 2017. T. 14. № 3. S. 42–47. (in Russian).
  2. Nikulina S.N., Cherikanova E.A., Chudakova T.A. Issledovaniye vliyaniya vybrosov avtotransporta v stolitse promyshlenno razvitogo regiona na zdorovye naseleniya. Naukoyemkiye tekhnologii. 2020. T. 21. № 9. S. 65–72. (in Russian).
  3. Krylova L.A., Yakovleva O.V. Puti rekonstruktsii i modernizatsii sooruzheniy biologicheskoy ochistki stoyachikh vod goroda. Naukoyemkiye tekhnologii. 2017. T. 18. № 6. S. 57–62. (in Russian).
  4. Hoang A.T. 2-Methylfuran (MF) as a potential biofuel: A thorough review on the production pathway from biomass, combustion progress, and application in engines. Renewable and Sustainable Energy Reviews. 2021. № 148. Р. 111265. https://doi.org/10.1016/ j.rser.2021.111265
  5. Sharipova N.U. Khimicheskaya promyshlennost i okruzhayushchaya sreda. Universum: khimiya i biologiya. 2022. № 5-1(95). S. 19–21. (in Russian).
  6. Niu Z., Liu F., Yu H., Wu S., Xiang H. Association between exposure to ambient air pollution and hospital admission, incidence, and mortality of stroke: an updated systematic review and meta-analysis of more than 23 million participants. Environmental health and preventive medicine. 2021. № 26(1). Р. 1–14. https://doi.org/10.1186/s12199-021-00937-1
  7. Crini G., Lichtfouse E. Advantages and disadvantages of techniques used for wastewater treatment. Environmental Chemistry Letters. 2019. № 17(1). Р. 145–155. https://doi.org/10.1007/s10311-018-0785-9
  8. Do M.H., Ngo H.H., Guo W.S., Liu Y., Chang S.W., Nguyen D.D. et al. Challenges in the application of microbial fuel cells to wastewater treatment and energy production: a mini review. Science of the Total Environment. 2018. № 639. P. 910–920. https://doi.org/10.1016/j.scitotenv.2018.05.136
  9. Guo Y., Wang J., Shinde S., Wang X., Li Y., Dai Y. et al. Simultaneous wastewater treatment and energy harvesting in microbial fuel cells: an update on the biocatalysts. RSC advances. 2020. № 10(43). Р. 25874–25887. https://doi.org/10.1039/D0RA05234E
  10. Din M.I., Nabi A.G., Hussain Z., Khalid R., Iqbal M., Arshad M. et al. Microbial fuel cells –A preferred technology to prevail energy crisis. International Journal of Energy Research. 2021. № 45(6). Р. 8370–8388. https://doi.org/10.1002/er.6403
  11. He L., Du P., Chen Y., Lu H., Cheng X., Chang B., Wang Z. Advances in microbial fuel cells for wastewater treatment. Renewable and Sustainable Energy Reviews. 2017. № 71. Р. 388–403. https://doi.org/10.1016/j.rser.2016.12.069
  12. Dubovets D.L. Mikrobnyy toplivnyy element kak istochnik alternativnoy energetiki. Problemy nauki. 2018. № 7(31). S. 26–28. (in Russian).
  13. Zamanpour M.K., Kariminia H.R., Vosoughi M. Electricity generation, desalination and microalgae cultivation in a biocathode-microbial desalination cell. Journal of Environmental Chemical Engineering. 2017. № 5(1). Р. 843–848. https://doi.org/10.1016/ j.jece.2016.12.045
  14. Lee H.S., Parameswaran P., Kato-Marcus A., Torres C.I., Rittmann B.E. Evaluation of energy-conversion efficiencies in microbial fuel cells (MFCs) utilizing fermentable and non-fermentable substrates. Water research. 2008. № 42(6-7). Р. 1501–1510. https://doi.org/10.1016/j.watres.2007.10.036
  15. Kim Y., Logan B.E. Microbial desalination cells for energy production and desalination. Desalination. 2013. № 308. Р. 122–130. https://doi.org/10.1016/j.desal.2012.07.022
  16. Chaudhary S., Yadav S., Singh R., Sadhotra C., Patil S.A. Extremophilic electroactive microorganisms: Promising biocatalysts for bioprocessing applications. Bioresource Technology. 2022. Р. 126663. https://doi.org/10.1016/j.biortech.2021.126663
  17. Cao Y., Mu H., Liu W., Zhang R., Guo J., Xian M., Liu H. Electricigens in the anode of microbial fuel cells: pure cultures versus mixed communities. Microbial cell factories. 2019. № 18(1). Р. 1–14. https://doi.org/10.1186/s12934-019-1087-z
  18. Thapa B.S., Kim T., Pandit S., Song Y.E., Afsharian Y.P., Rahimnejad M. et al. Overview of electroactive microorganisms and electron transfer mechanisms in microbial electrochemistry. Bioresource Technology. 2021. Р. 126579. https://doi.org/10.1016/j.biortech.2021.126579
  19. Aiyer K.S. How does electron transfer occur in microbial fuel cells?. World Journal of Microbiology and Biotechnology. 2020. № 36(2). Р. 1–9. https://doi.org/10.1007/s11274-020-2801-z
  20. Kumar A., Hsu L.H.H., Kavanagh P., Barrière F., Lens P.N., Lapinsonnière L. et al. The ins and outs of microorganism–electrode electron transfer reactions. Nature Reviews Chemistry. 2017. № 1(3). Р. 1–13. https://doi.org/10.1038/s41570-017-0024
  21. Costa N.L., Clarke T.A., Philipp L.A., Gescher J., Louro R.O., Paquete C.M. Electron transfer process in microbial electrochemical technologies: the role of cell-surface exposed conductive proteins. Bioresource technology. 2018. № 255. Р. 308–317. https://doi.org/10.1016/j.biortech.2018.01.133
  22. Ranieri A., Borsari M., Casalini S., Di Rocco G., Sola M., Bortolotti C.A., Battistuzzi G. How to turn an electron transfer protein into a redox enzyme for biosensing. Molecules. 2021. № 26(16). P. 4950. https://doi.org/10.3390/molecules26164950
  23. Bhat A.H., Nguyen M.T., Das A., Ton-That H. Anchoring surface proteins to the bacterial cell wall by sortase enzymes: how it started and what we know now. Current Opinion in Microbiology. 2021. № 60. Р. 73–79. https://doi.org/10.1016/j.mib.2021.01.013
  24. Shi M., Jiang Y., Shi L. Electromicrobiology and biotechnological applications of the exoelectrogens Geobacter and Shewanella spp.. Science China Technological Sciences. 2019. № 62(10). P. 1670–1678. https://doi.org/10.1007/s11431-019-9509-8
  25. You L.X., Liu L.D., Xiao Y., Dai Y.F., Chen B.L., Jiang Y.X., Zhao F. Flavins mediate extracellular electron transfer in Gram-positive Bacillus megaterium strain LLD-1. Bioelectrochemistry. 2018. № 119. Р. 196–202. https://doi.org/10.1016/j.bioelechem.2017.10.005
  26. Brutinel E.D., Gralnick J.A. Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Applied microbiology and biotechnology. 2012. № 93(1). Р. 41–48. https://doi.org/10.1007/s00253-011-3653-0
  27. Marsili E., Baron D.B., Shikhare I.D., Coursolle D., Gralnick J.A., Bond D.R. Shewanella secretes flavins that mediate extracellular electron transfer. Proceedings of the National Academy of Sciences. 2008. № 105(10). Р. 3968–3973. https://doi.org/10.1073/pnas.0710525105
  28. Saralov A.I. Adaptivity of archaeal and bacterial extremophiles. Microbiology. 2019. № 88(4). Р. 379–401. https://doi.org/10.1134/S0026261719040106
  29. Abrevaya C., Sacco N., Mauas P.J., Cortón E.X. Archaea-based microbial fuel cell operating at high ionic strength conditions. Extremophiles. 2011. № 15(6). Р. 633–642. https://doi.org/10.1007/s00792-011-0394-z
  30. Kaminskaya O.P., Semenov A.Yu. Sotrudnichestvo s Aleksandrom Konstantinovym v issledovanii mekhanizmov elektrogennykh reaktsiy v bakterialnykh fotosinteticheskikh reaktsionnykh tsentrakh. Biokhimiya. 2021. T. 86. № 1. S. 6–13. (in Russian).
  31. Berk R.S., Canfield J.H. Bioelectrochemical energy conversion. Applied microbiology. 1964. № 12(1). Р. 10–12.
  32. Borole A.P., O’Neill H., Tsouris C., Cesar S. А microbial fuel cell operating at low pH using the acidophile Acidiphilium cryptum. Biotechnology letters. 2008. № 30(8). Р. 1367–1372. https://doi.org/10.1007/s10529-008-9700-y
  33. Chaudhuri S.K., Lovley D.R. Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nature biotechnology. 2003. № 21(10). Р. 1229–1232. https://doi.org/10.1038/nbt867
  34. Liu Z.D., Li H.R. Effects of bio- and abio-factors on electricity production in a mediatorless microbial fuel cell. Biochem. Eng. J. 2007. № 36. Р. 209–214. https://doi.org/10.1016/j.bej.2007.02.021
  35. Shah S., Venkatramanan V., Prasad R. Microbial fuel cell: Sustainable green technology for bioelectricity generation and wastewater treatment. Sustainable Green Technologies for Environmental Management. 2019. Р. 199–218. https://doi.org/10.1007/978-981-13-2772-8_10
  36. Logan B.E., Rossi R., Ragab A., Saikaly P.E. Electroactive microorganisms in bioelectrochemical systems. Nature Reviews Microbiology. 2019. № 17(5). Р. 307–319. https://doi.org/10.1038/s41579-019-0173-x
  37. Li H., Liao B., Xiong J., Zhou X., Zhi H., Liu X. et al. Power output of microbial fuel cell emphasizing interaction of anodic binder with bacteria. Journal of Power Sources. 2018. № 379. Р. 115–122. https://doi.org/10.1016/j.jpowsour.2018.01.040
  38. Xiang K., Qiao Y., Ching C.B., Li C.M. GldA overexpressing-engineered E. coli as superior electrocatalyst for microbial fuel cells. Electrochemistry Communications. 2009. № 11(8). Р. 1593–1595. https://doi.org/10.1016/j.elecom.2009.06.004
  39. You T., Liu J., Liang R. Survival elongation of Pseudomonas aeruginosa improves power output of microbial fuel cells. Sheng wu Gong Cheng xue bao-Chinese Journal of Biotechnology. 2017. № 33(4). Р. 601–608. https://doi.org/10.13345/j.cjb.160372
  40. Yong X.Y., Yan Z.Y., Shen H.B., Zhou J., Wu X.Y., Zhang L.J. An integrated aerobic-anaerobic strategy for performance enhancement of Pseudomonas aeruginosa-inoculated microbial fuel cell. Bioresource Technology. 2017. № 241. P. 1191–1196. https://doi.org/10.1016/j.biortech.2017.06.050
  41. Ilamathi R., Sheela A.M., Gandhi N.N. Comparative evaluation of Pseudomonas species in single chamber microbial fuel cell with manganese coated cathode for reactive azo dye removal. International Biodeterioration & Biodegradation. 2019. № 144. Р. 104744. https://doi.org/10.1016/j.ibiod.2019.104744
  42. Lemaire O.N., Méjean V., Iobbi-Nivol C. The Shewanella genus: ubiquitous organisms sustaining and preserving aquatic ecosystems. FEMS Microbiology Reviews. 2020. № 44(2). P. 155–170. https://doi.org/10.1093/femsre/fuz031
  43. Zou L., Lu Z., Huang Y., Long Z.E., Qiao Y. Nanoporous Mo2C functionalized 3D carbon architecture anode for boosting flavins mediated interfacial bioelectrocatalysis in microbial fuel cells. Journal of Power Sources. 2017. № 359. Р. 549–555. https://doi.org/10.1016/j.jpowsour.2017.05.101
  44. Zou L., Qiao Y., Zhong C., Li C.M. 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. 2017. № 229. Р. 31–38. https://doi.org/10.1016/j.electacta.2017.01.081
  45. Newton G.J., Mori S., Nakamura R., Hashimoto K., Watanabe K. Analyses of current-generating mechanisms of Shewanella loihica PV-4 and Shewanella oneidensis MR-1 in microbial fuel cells. Applied and Environmental Microbiology. 2009. № 75(24). Р. 7674–7681. https://doi.org/10.1128/AEM.01142-09
  46. Wu X., Zou L., Huang Y., Qiao Y., Long Z.E., Liu H., Li C.M. Shewanella putrefaciens CN32 outer membrane cytochromes MtrC and UndA reduce electron shuttles to produce electricity in microbial fuel cells. Enzym Microb Technol. 2018. № 115. Р. 23–28. https://doi.org/10.1016/j.enzmictec.2018.04.005
  47. Li S.W., Zeng R.J., Sheng G.P. An excellent anaerobic respiration mode for chitin degradation by Shewanella oneidensis MR-1 in microbial fuel cells. Biochemical Engineering Journal. 2017. № 118. Р. 20–24. https://doi.org/10.1016/j.bej.2016.11.010
  48. Stöckl M., Teubner N.C., Holtmann D., Mangold K.M., Sand W. Extracellular polymeric substances from Geobacter sulfurreducens biofilms in microbial fuel cells. ACS applied materials & interfaces. 2019. № 11(9). Р. 8961–8968. https://doi.org/10.1021/acsami.8b14340
  49. Vasconcelos B., Teixeira J.C., Dragone G., Teixeira J.A. Oleaginous yeasts for sustainable lipid production—from biodiesel to surf boards, a wide range of “green” applications. Applied microbiology and biotechnology. 2019. № 103(9). Р. 3651–3667. https://doi.org/10.1007/s00253-019-09742-x
  50. Verma M., Mishra V. Recent trends in upgrading the performance of yeast as electrode biocatalyst in microbial fuel cells. Chemosphere. 2021. № 284. Р. 131383. https://doi.org/10.1016/j.chemosphere.2021.131383
  51. Sahu O. Sustainable and clean treatment of industrial wastewater with microbial fuel cell. Results in Engineering. 2019. № 4. Р. 100053. https://doi.org/10.1016/j.rineng.2019.100053
  52. Hanzhola G., Tribidasari A.I., Endang S. The use of boron-doped diamond electrode on yeast-based microbial fuel cell for electricity production. In Journal of Physics: Conference Series. 2018. № 953(1). Р. 012005. https://doi.org/10.1088/1742-6596/953/1/012005
  53. Islam M.A., Ethiraj B., Cheng C.K., Yousuf A., Thiruvenkadam S., Prasad R., Rahman Khan M.M. Enhanced current generation using mutualistic interaction of yeast-bacterial coculture in dual chamber microbial fuel cell. Industrial & Engineering Chemistry Research. 2018. № 57(3). Р. 813–821. https://doi.org/10.1021/acs.iecr.7b01855
  54. Sarmin S., Tarek M., Roopan S.M., Cheng C.K., Khan M.M.R. Significant improvement of power generation through effective substrate-inoculum interaction mechanism in microbial fuel cell. Journal of Power Sources. 2021. № 484. Р. 229285. https://doi.org/10.1016/j.jpowsour.2020.229285
  55. Lin T., Bai X., Hu Y., Li B., Yuan Y.J., Song H. Synthetic Saccharomyces cerevisiae‐Shewanella oneidensis consortium enables glucose‐fed high‐performance microbial fuel cell. AIChE Journal. 2017. № 63(6). Р. 1830–1838. https://doi.org/10.1002/aic.15611
  56. Liu S.H., Tsai S.L., Guo P.Y., Lin C.W. Inducing laccase activity in white rot fungi using copper ions and improving the efficiency of azo dye treatment with electricity generation using microbial fuel cells. Chemosphere. 2020. № 243. Р. 125304. https://doi.org/10.1016/j.chemosphere.2019.125304
  57. Zhang L., Cui H., Dhoke G.V., Zou Z., Sauer D.F., Davari M.D., Schwaneberg U. Engineering of Laccase CueO for Improved Electron Transfer in Bioelectrocatalysis by Semi‐Rational Design. Chemistry – A European Journal. 2020. № 26(22). Р. 4974–4979. https://doi.org/10.1002/chem.201905598
  58. Lai C.Y., Wu C.H., Meng C.T., Lin C.W. Decolorization of azo dye and generation of electricity by microbial fuel cell with laccase-producing white-rot fungus on cathode. Applied Energy. 2017. № 188. Р. 392–398. https://doi.org/10.1016/j.apenergy.2016.12.044
  59. Simões M.F., Maiorano A.E., dos Santos J.G., Peixoto L., de Souza R.F.B., Neto A.O. Microbial fuel cell-induced production of fungal laccase to degrade the anthraquinone dye Remazol Brilliant Blue R. Environmental Chemistry Letters. 2019. № 7(3). Р. 1413–1420. https://doi.org/10.1007/s10311-019-00876-y
  60. Lin C.W., Wu C.H., Lin Y.Y., Liu S.H., Chang S.H. Enhancing the performance of microbial fuel cell using a carbon-fiber-brush air cathode with low-cost mushroom Ganoderma laccase enzyme. Journal of the Taiwan Institute of Chemical Engineers. 2018. № 85. Р. 115–120. https://doi.org/10.1016/j.jtice.2017.12.025
  61. Lin C.W., Lai C.Y., Liu S.H., Chen Y.R., Alfanti L.K. Enhancing bioelectricity generation and removal of copper in microbial fuel cells with a laccase-catalyzed biocathode. Journal of Cleaner Production. 2021. № 298. Р. 126726. https://doi.org/10.1016/j.jclepro.2021.126726
  62. Jaiswal K.K., Banerjee I., Singh D., Sajwan P., Chhetri V. Ecological stress stimulus to improve microalgae biofuel generation: a review. Octa J. Biosci. 2020. № 8. Р. 48–54.
  63. Li Y., Horsman M., Wu N., Lan C.Q., Dubois‐Calero N. Biofuels from microalgae. Biotechnology progress. 2008. № 24(4). Р. 815–820.
  64. Ashwaniy V.R.V., Perumalsamy M. Reduction of organic compounds in petro-chemical industry effluent and desalination using Scenedesmus abundans algal microbial desalination cell. Journal of environmental chemical engineering. 2017. №5(6). Р. 5961–5967. https://doi.org/10.1016/j.jece.2017.11.017
  65. Mohamed S.N., Jayabalan T., Muthukumar K. Simultaneous bioenergy generation and carbon dioxide sequestration from food wastewater using algae microbial fuel cell. Energy Sources, Part A: Recovery, Utilization, and Environmental Effects. 2019. Р. 1–9. https://doi.org/10.1080/15567036.2019.1666932
  66. Abazarian E., Gheshlaghi R., Mahdavi M.A. Impact of light/dark cycle on electrical and electrochemical characteristics of algal cathode sediment microbial fuel cells. Journal of Power Sources. 2020. № 475. Р. 228686. https://doi.org/10.1016/j.jpowsour.2020.228686
  67. Bazdar E., Roshandel R., Yaghmaei S., Mardanpour M.M. The effect of different light intensities and light/dark regimes on the performance of photosynthetic microalgae microbial fuel cell. Bioresource technology. 2018. № 261. Р. 350–360. https://doi.org/10.1016/j.biortech.2018.04.026
Date of receipt: 28.07.2022
Approved after review: 11.09.2022
Accepted for publication: 25.10.2022