Microbial electroactive biofilms dominated by Geoalkalibacter spp. from a highly saline–alkaline environment
1.
Lovley, D. R. Electromicrobiology. Annu. Rev. Microbiol 66, 391–409 (2012).
CAS PubMed Article Google Scholar
2.
Nealson, K. H. & Rowe, A. R. Electromicrobiology: realities, grand challenges, goals, and predictions. Micro. Biotechnol. 9, 595–600 (2016).
Article Google Scholar
3.
Nealson, K. H. Bioelectricity (electromicrobiology) and sustainability. Micro. Biotechnol. 10, 1114–1119 (2017).
CAS Article Google Scholar
4.
Logan, B. E., Rossi, R., Ragab, A. & Saikaly, P. E. Electroactive microorganisms in bioelectrochemical systems. Nat. Rev. Microbiol 17, 307–319 (2019).
CAS PubMed Article Google Scholar
5.
Lonergan, D. J. et al. Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria. J. Bacteriol. 178, 2402–2408 (1996).
CAS PubMed PubMed Central Article Google Scholar
6.
Lovley, D. R., Phillips, E. J. P., Caccavo, F., Nealson, K. H. & Myers, C. Acetate oxidation by dissimilatory Fe(III) reducers. Appl. Environ. Microbiol 58, 3205–3208 (1992).
CAS PubMed PubMed Central Article Google Scholar
7.
Myers, C. R., Nealson, K. H. & June, I. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240, 1319–1322 (1988).
CAS PubMed Article Google Scholar
8.
Rotaru, A. E. et al. A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ. Sci. 7, 408–415 (2014).
CAS Article Google Scholar
9.
Kato, S., Hashimoto, K. & Watanabe, K. Microbial interspecies electron transfer via electric currents through conductive minerals. Proc. Natl Acad Sci. USA 109, 10042–10046 (2012).
CAS PubMed Article Google Scholar
10.
Katuri, K. P. et al. Dual-function electrocatalytic and macroporous hollow fiber cathode for converting water streams to valuable resources using microbial electrochemical systems. Adv. Mater. 30, 1707072 (2018).
Article CAS Google Scholar
11.
Pandey, P. et al. Recent advances in the use of different substrates in microbial fuel cells toward wastewater treatment and simultaneous energy recovery. Appl. Energ. 168, 706–723 (2016).
CAS Article Google Scholar
12.
Chiranjeevi, P. & Patil, S. A. Strategies for improving the electroactivity and specific metabolic functionality of microorganisms for various microbial electrochemical technologies. Biotechnol. Adv. 39, 107468 (2020).
13.
Kiran, R. & Patil, S. A. in Introduction to Biofilm Engineering, Vol. 1323 (eds Rathinam, N. K. & Sani, R. K.) 159–186 (ACS: Symposium Series, 2019).
14.
Rowe, A. R. et al. In situ electrochemical enrichment and isolation of a magnetite-reducing bacterium from a high pH serpentinizing spring. Environ. Microbiol. 19, 2272–2285 (2017).
CAS PubMed Article Google Scholar
15.
Shrestha, N. et al. Extremophiles for microbial-electrochemistry applications: a critical review. Bioresour. Technol. 255, 318–330 (2018).
CAS PubMed Article Google Scholar
16.
Dopson, M., Ni, G. & Sleutels, T. H. J. A. Possibilities for extremophilic microorganisms in microbial electrochemical systems. FEMS Microbiol. Rev. 40, 164–181 (2016).
CAS PubMed Article Google Scholar
17.
Pierra, M., Carmona-martínez, A. A., Trably, E., Godon, J. & Bernet, N. Bioelectrochemistry specific and efficient electrochemical selection of Geoalkalibacter subterraneus and Desulfuromonas acetoxidans in high current-producing biofilms. Bioelectrochemistry 106, 182–189 (2015).
Article CAS Google Scholar
18.
Alqahtani, M. F. et al. Enrichment of Marinobacter sp. and halophilic homoacetogens at biocathode of microbial electrosynthesis systems inoculated with Red-Sea brine pool. Front. Microbiol. 109, 2563 (2019).
Article Google Scholar
19.
Shehab et al. Enrichment of extremophilic exoelectrogens in microbial electrolysis cells using Red Sea brine pools as inocula. Bioresour. Technol. 239, 82–86 (2017).
CAS PubMed Article Google Scholar
20.
Sulonen, M. L. K., Kokko, M. E., Lakaniemi, A. & Puhakka, J. A. Electricity generation from tetrathionate in microbial fuel cells by acidophiles. J. Hazard Mater. 284, 182–189 (2015).
CAS PubMed Article Google Scholar
21.
Badalamenti, J. P., Krajmalnik-Brown, R. & Torres, I. Generation of high current densities by pure cultures of anode-respiring Geoalkalibacter spp. under alkaline and saline conditions in microbial electrochemical cells. mBio 4, e00144–13 (2013).
CAS PubMed PubMed Central Article Google Scholar
22.
Holmes, D. E., Nicoll, J. S., Bond, D. R. & Lovley, D. R. Potential role of a novel psychrotolerant member of the family Geobacteraceae, Geopsychrobacter electrodiphilus gen. nov., sp. nov., in electricity production by a marine sediment fuel cell. Appl. Environ. Microbiol. 75, 885 (2009).
CAS PubMed Central Article PubMed Google Scholar
23.
Parameswaran, P., Bry, T., Popat, S. C., Lusk, B. G. & Rittmann, B. E. Kinetic, electrochemical, and microscopic characterization of the thermophilic, anode-respiring bacterium Thermincola ferriacetica. Environ. Sci. Technol. 47, 4934–4940 (2013).
CAS PubMed Article Google Scholar
24.
Pillot, G. et al. Specific enrichment of hyperthermophilic electroactive Archaea from a deep-sea hydrothermal vent on electrically conductive support. Bioresour. Technol. 259, 304–311 (2018).
CAS PubMed Article Google Scholar
25.
Cerqueira, T. et al. Sediment microbial diversity of three deep-sea hydrothermal vents southwest of the azores. Micro. Ecol. 74, 332–349 (2017).
CAS Article Google Scholar
26.
Jangir, Y. et al. In situ electrochemical studies of the terrestrial deep subsurface biosphere at the Sanford Underground Research Facility, South Dakota, USA. Front Energy Res 7, 1–17 (2019).
Article Google Scholar
27.
Carmona-Martinez, A. A., Pierra, M., Trably, E. & Bernet, N. High current density via direct electron transfer by the halophilic anode respiring bacterium Geoalkalibacter subterraneus. Phys. Chem. Chem. Phys. 15, 19699–19707 (2013).
CAS PubMed Article Google Scholar
28.
Abrevaya, X. C., Sacco, N., Mauas, P. J. D. & Cortón, E. Archaea-based microbial fuel cell operating at high ionic strength conditions. Extremophiles 15, 633–642 (2011).
CAS PubMed Article Google Scholar
29.
Ledezma, P., Lu, Y. & Freguia, S. Electroactive haloalkaliphiles exhibit exceptional tolerance to free ammonia. FEMS Microbiol. Lett. 365, 1–6 (2018).
Article CAS Google Scholar
30.
Kumar, S. K., Feria, S. O., Ramírez, T. J., Seijas, R. N. & Varaldo, P. H. M. Electrochemical, and chemical enrichment methods of a sodic-saline inoculum for microbial fuel cells. Int. J. Hydrog. Energy 38, 12600–12609 (2013).
Article CAS Google Scholar
31.
Borul, S. B. Study of water quality of Lonar Lake. J. Chem. Pharm. Res. 4, 1716–1718 (2012).
CAS Google Scholar
32.
Jadhav, R. D. & Mali, H. B. A search for the source of high content of sodium chloride (NaCl) at Crater Lake Lonar, Maharashtra, India. Int. J. Adv. Res. Ideas Innov. Technol. 4, 255–261 (2018).
Google Scholar
33.
Wani, A. A. et al. Molecular analyses of microbial diversity associated with the Lonar soda lake in India: an impact crater in a basalt area. Res. Microbiol. 157, 928–937 (2006).
CAS PubMed Article Google Scholar
34.
Joshi, A. A. et al. Cultivable bacterial diversity of alkaline Lonar Lake. India Microbiol. Ecol. 55, 163–172 (2008).
Article Google Scholar
35.
Paul, D. et al. Exploration of microbial diversity and community structure of Lonar Lake: the only hypersaline meteorite Crater Lake within basalt rock. Front. Microbiol. 6, 1–12 (2016).
Article Google Scholar
36.
Misra, S. et al. Geochemical identification of impactor for Lonar crater, India. Meteorit. Planet Sci. 1018, 1001–1018 (2009).
Article Google Scholar
37.
Koshy, N. et al. Characterization of the soil samples from the Lonar crater. India Geotech. Eng. 49, 99–105 (2018).
Google Scholar
38.
Yee, M. O., Deutzmann, J., Spormann, A. & Rotaru, A. Cultivating electroactive microbes—from field to bench. Nanotechnology 31, 174003 (2020).
CAS PubMed Article Google Scholar
39.
Korth, B. & Harnisch, F. Spotlight on the energy harvest of electroactive microorganisms: the impact of the applied anode potential. Front. Microbiol. 10, 1–9 (2019).
Article Google Scholar
40.
Parot, S., Delia, M. L. & Bergel, A. Forming electrochemically active biofilms from garden compost under chronoamperometry. Bioresour. Technol. 99, 4809–4816 (2008).
CAS PubMed Article Google Scholar
41.
Torres, C. I. et al. Selecting anode-respiring bacteria based on anode potential: phylogenetic, electrochemical, and microscopic characterization. Environ. Sci. Technol. 43, 9519–9524 (2009).
CAS PubMed Article Google Scholar
42.
Babu, P., Chandel, A. K. & Singh, O. V. in Extremophiles and Their Applications in Medical Processes (eds Babu, P., Chandel, A. K. & Singh, O.V.) 9–24 (Springer, 2015).
43.
Harnisch, F. & Freguia, S. A basic tutorial on cyclic voltammetry for the investigation of electroactive microbial biofilms. Chem. Asian J. 7, 466–475 (2012).
CAS PubMed Article Google Scholar
44.
Peng, L. et al. Geobacter sulfurreducens adapts to low electrode potential for extracellular electron transfer. Electrochim. Acta 191, 743–749 (2016).
CAS Article Google Scholar
45.
Marsili, E., Sun, J. & Bond, D. R. Voltammetry and growth physiology of Geobacter sulfurreducens biofilms as a function of the growth stage and imposed electrode potential. Electroanalysis 22, 865–874 (2010).
CAS Article Google Scholar
46.
Yoho, R. A., Popat, S. C., Rago, L. & Guisasola, A. Anode biofilms of Geoalkalibacter ferrihydriticus exhibit electrochemical signatures of multiple electron transport pathways. Langmuir 31, 12552–12559 (2015).
CAS PubMed Article Google Scholar
47.
Schroder, U. & Harnisch, F. In Encyclopedia of Applied Electrochemistry (eds Kreysa, G., Ota, K. & Savinell, R. F.) 120–126 (Springer, New York, 2014).
48.
Patil, S. A., Harnisch, F., Kapadnis, B. & Schröder, U. Electroactive mixed culture biofilms in microbial bioelectrochemical systems: The role of temperature on the formation and performance. Biosens. Bioelectron. 26, 803–808 (2010).
CAS PubMed Article Google Scholar
49.
Liu, Y., Climent, V., Berná, A. & Feliu, J. M. Effect of temperature on the catalytic ability of electrochemically active biofilm as anode catalyst in microbial fuel cells. Electroanalysis 23, 387–394 (2011).
CAS Article Google Scholar
50.
Huang, L., Hwang, A. & Phillips, J. Effect of temperature on microbial growth rate-mathematical analysis: the Arrhenius and Eyring-Polanyi connections. J. Food Sci. 76, 553–560 (2011).
Article CAS Google Scholar
51.
Labelle, E. & Bond, D. R. In Bioelectrochemical Systems: From Extracellular Electron Transfer to Biotechnological Applications (eds Rabaey, K., Angenent, I., Schroder, U. & Keller, J.) 137–152 (IWA Publishing, London, 2005).
52.
Patil, S. A., Hägerhäll, C. & Gorton, L. Electron transfer mechanisms between microorganisms and electrodes in bioelectrochemical systems. Bio Anal. Rev. 4, 159–192 (2012).
Article Google Scholar
53.
Richter, H. et al. Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer. Energy Environ. Sci. 2, 506–516 (2009).
CAS Article Google Scholar
54.
Katuri, K. P., Rengaraj, S., Kavanagh, P., O’Flaherty, V. & Leech, D. Charge transport through Geobacter sulfurreducens biofilms grown on graphite rods. Langmuir 28, 7904–7913 (2012).
CAS PubMed Article Google Scholar
55.
Fricke, K., Harnisch, F. & Schroder, U. On the use of cyclic voltammetry for the study of anodic electron transfer in microbial fuel cells. Energy Environ. Sci. 1, 144–147 (2008).
CAS Article Google Scholar
56.
Harnisch, F. et al. Revealing the electrochemically driven selection in natural community derived microbial biofilms using flow-cytometry. Energy Environ. Sci. 4, 1265–1267 (2011).
CAS Article Google Scholar
57.
Carmona-Martinez, A. A. et al. Cyclic voltammetric analysis of the electron transfer of Shewanella oneidensis MR-1 and nanofilament and cytochrome knock-out mutants. Bioelectrochemistry 81, 74–80 (2011).
CAS PubMed Article Google Scholar
58.
Firer-Sherwood, M., Pulcu, G. S. & Elliott, S. J. Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window. J. Biol. Inorg. Chem. 13, 849–854 (2008).
CAS PubMed Article Google Scholar
59.
Baron, D., LaBelle, E., Coursolle, D., Gralnick, J. A. & Bond, D. R. Electrochemical measurement of electron transfer kinetics by Shewanella oneidensis MR-1. J. Biol. Chem. 284, 28865–28873 (2009).
CAS PubMed PubMed Central Article Google Scholar
60.
Holmes, D. E., Nevin, K. P. & Lovley, D. R. Comparison of nifD, recA, gyrB and fusA genes within the family Geobacteraceae Fam. nov. Int. J. Syst. Evol. Microbiol 54, 1591–1599 (2004).
CAS PubMed Article Google Scholar
61.
Greene, A. C., Patel, B. K. C. & Yacob, S. Anaerobic Fe (III) – and Mn (IV) -reducing bacterium from a petroleum reservoir, and emended descriptions of the family Desulfuromonadaceae and the genus Geoalkalibacter. Int. J. Syst. Evol. Microbiol. 59, 781–785 (2009).
CAS PubMed Article Google Scholar
62.
Badalamenti, J. P., Summers, Z. M., Chan, C. H., Gralnick, J. A. & Bond, D. R. Isolation and genomic characterization of ‘Desulfuromonas soudanensis WTL’, a metal- and electrode-respiring bacterium from anoxic deep subsurface brine. Front. Microbiol. 7, 1–11 (2016).
Article Google Scholar
63.
Jayashree, C., Tamilarasan, K., Rajkumar, M., Arulazhagan, P. & Yogalakshmi, K. N. Treatment of seafood processing wastewater using up-flow microbial fuel cell for power generation and identification of bacterial community in anodic biofilm. J. Environ. Manag. 180, 351–358 (2016).
CAS Article Google Scholar
64.
Monzon, O. et al. Microbial fuel cell fed by Barnett Shale produced water: power production by hypersaline autochthonous bacteria and coupling to a desalination unit. Biochem. Eng. J. 117, 87–91 (2017).
CAS Article Google Scholar
65.
Kevbrin, V. V., Zhilina, T. N., Rainey, F. A. & Zavarzin, G. A. Tindallia magadii gen. nov., sp. nov.: an alkaliphilic anaerobic ammonifier from Soda Lake deposits. Curr. Microbiol. 37, 94–100 (1998).
CAS PubMed Article Google Scholar
66.
Mei, N. et al. Serpentinicella alkaliphila gen. nov., sp. nov., a novel alkaliphilic anaerobic bacterium isolated from the serpentinite-hosted Prony hydrothermal field, New Caledonia. Int. J. Syst. Evol. Microbiol. 66, 4464–4470 (2016).
CAS PubMed Article Google Scholar
67.
Pasupuleti, S. B., Srikanth, S., Dominguez-Benetton, X., Mohan, S. V. & Pant, D. Dual gas diffusion cathode design for Microbial Fuel Cell (MFC): optimizing the suitable mode of operation in terms of biochemical & bioelectro-kinetic evaluation. J. Chem. Technol. Biotechnol. 91, 624–639 (2016).
CAS Article Google Scholar
68.
Srikanth, S. et al. Electro-biocatalytic conversion of carbon dioxide to alcohols using gas diffusion electrodes. Bioresour. Technol. 265, 45–51 (2018).
CAS PubMed Article Google Scholar
69.
Patil, S. A. et al. Electroactive mixed culture derived biofilms in microbial bioelectrochemical systems: the role of pH on biofilm formation, performance, and composition. Bioresour. Technol. 102, 9683–9690 (2011).
CAS PubMed Article Google Scholar
70.
Feng, Y., Yang, Q., Wang, X. & Logan, B. E. Treatment of carbon fiber brush anodes for improving power generation in air-cathode microbial fuel cells. J. Power Sources 195, 1841–1844 (2010).
CAS Article Google Scholar More