Electroactive biofilms: how microbial electron transfer enables bioelectrochemical applications

Conners, Eric M.; Rengasamy, Karthikeyan; Bose, Arpita

doi:10.1093/jimb/kuac012

Title: Electroactive biofilms: how microbial electron transfer enables bioelectrochemical applications

Journal Article · 05 April 2022 · Journal of Industrial Microbiology and Biotechnology

DOI: https://doi.org/10.1093/jimb/kuac012 · OSTI ID:1879114

; Rengasamy, Karthikeyan; Bose, Arpita

Abstract Microbial biofilms are ubiquitous. In marine and freshwater ecosystems, microbe–mineral interactions sustain biogeochemical cycles, while biofilms found on plants and animals can range from pathogens to commensals. Moreover, biofouling and biocorrosion represent significant challenges to industry. Bioprocessing is an opportunity to take advantage of biofilms and harness their utility as a chassis for biocommodity production. Electrochemical bioreactors have numerous potential applications, including wastewater treatment and commodity production. The literature examining these applications has demonstrated that the cell–surface interface is vital to facilitating these processes. Therefore, it is necessary to understand the state of knowledge regarding biofilms’ role in bioprocessing. This mini-review discusses bacterial biofilm formation, cell–surface redox interactions, and the role of microbial electron transfer in bioprocesses. It also highlights some current goals and challenges with respect to microbe-mediated bioprocessing and future perspectives.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC52-07NA27344; SC0014613

OSTI ID:: 1879114

Journal Information:: Journal of Industrial Microbiology and Biotechnology, Journal Name: Journal of Industrial Microbiology and Biotechnology Journal Issue: 4 Vol. 49; ISSN 1367-5435

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: Germany

Language:: English

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Biofilm and Nanowire Production Leads to Increased Current in Geobacter sulfurreducens Fuel Cells Reguera, G.; Nevin, K. P.; Nicoll, J. S. Applied and Environmental Microbiology, Vol. 72, Issue 11 https://doi.org/10.1128/AEM.01444-06	journal	August 2006
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 Liu, Xing; Tremblay, Pier-Luc; Malvankar, Nikhil S. Applied and Environmental Microbiology, Vol. 80, Issue 3 https://doi.org/10.1128/AEM.02938-13	journal	December 2013
A Previously Uncharacterized, Nonphotosynthetic Member of the Chromatiaceae Is the Primary CO ₂ -Fixing Constituent in a Self-Regenerating Biocathode Wang, Zheng; Leary, Dagmar H.; Malanoski, Anthony P. Applied and Environmental Microbiology, Vol. 81, Issue 2 https://doi.org/10.1128/AEM.02947-14	journal	November 2014
Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens Mehta, T.; Coppi, M. V.; Childers, S. E. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8634-8641.2005	journal	December 2005
Heterogeneity in Pseudomonas aeruginosa Biofilms Includes Expression of Ribosome Hibernation Factors in the Antibiotic-Tolerant Subpopulation and Hypoxia-Induced Stress Response in the Metabolically Active Population Williamson, Kerry S.; Richards, Lee A.; Perez-Osorio, Ailyn C. Journal of Bacteriology, Vol. 194, Issue 8 https://doi.org/10.1128/JB.00022-12	journal	April 2012
The pio Operon Is Essential for Phototrophic Fe(II) Oxidation in Rhodopseudomonas palustris TIE-1 Jiao, Y.; Newman, D. K. Journal of Bacteriology, Vol. 189, Issue 5 https://doi.org/10.1128/JB.00776-06	journal	December 2006
The Mtr Respiratory Pathway Is Essential for Reducing Flavins and Electrodes in Shewanella oneidensis Coursolle, D.; Baron, D. B.; Bond, D. R. Journal of Bacteriology, Vol. 192, Issue 2 https://doi.org/10.1128/JB.00925-09	journal	November 2009
OmcB, a c-Type Polyheme Cytochrome, Involved in Fe(III) Reduction in Geobacter sulfurreducens Leang, C.; Coppi, M. V.; Lovley, D. R. Journal of Bacteriology, Vol. 185, Issue 7 https://doi.org/10.1128/JB.185.7.2096-2103.2003	journal	April 2003
Anaerobic Growth of Thiobacillus ferrooxidans Pronk, J. T.; de Bruyn, J. C.; Bos, P. Applied and Environmental Microbiology, Vol. 58, Issue 7 https://doi.org/10.1128/aem.58.7.2227-2230.1992	journal	July 1992
Extracellular Enzymes Facilitate Electron Uptake in Biocorrosion and Bioelectrosynthesis Deutzmann, Jörg S.; Sahin, Merve; Spormann, Alfred M. mBio, Vol. 6, Issue 2 https://doi.org/10.1128/mBio.00496-15	journal	April 2015
An Inner Membrane Cytochrome Required Only for Reduction of High Redox Potential Extracellular Electron Acceptors Levar, Caleb E.; Chan, Chi Ho; Mehta-Kolte, Misha G. mBio, Vol. 5, Issue 6 https://doi.org/10.1128/mBio.02034-14	journal	November 2014
Methane-Linked Mechanisms of Electron Uptake from Cathodes by Methanosarcina barkeri Rowe, Annette R.; Xu, Shuai; Gardel, Emily mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mBio.02448-18	journal	March 2019
Photoferrotrophs Produce a PioAB Electron Conduit for Extracellular Electron Uptake Gupta, Dinesh; Sutherland, Molly C.; Rengasamy, Karthikeyan mBio, Vol. 10, Issue 6 https://doi.org/10.1128/mBio.02668-19	journal	November 2019
Metatranscriptomics Supports the Mechanism for Biocathode Electroautotrophy by “Candidatus Tenderia electrophaga” Eddie, Brian J.; Wang, Zheng; Hervey, W. Judson mSystems, Vol. 2, Issue 2 https://doi.org/10.1128/mSystems.00002-17	journal	March 2017
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A new mathematical model of bacterial interactions in two-species oral biofilms Martin, Bénédicte; Tamanai-Shacoori, Zohreh; Bronsard, Julie PLOS ONE, Vol. 12, Issue 3 https://doi.org/10.1371/journal.pone.0173153	journal	March 2017
Poly(3-hydroxybutyrate) production in an integrated electromicrobial setup: Investigation under stress-inducing conditions Al Rowaihi, Israa Salem; Paillier, Alexis; Rasul, Shahid PLOS ONE, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pone.0196079	journal	April 2018
What are the advantages of living in a community? A microbial biofilm perspective! Santos, André Luis Souza dos; Galdino, Anna Clara Milesi; Mello, Thaís Pereira de Memórias do Instituto Oswaldo Cruz, Vol. 113, Issue 9 https://doi.org/10.1590/0074-02760180212	journal	January 2018
Production and characterization of poly-3-hydroxybutyrate from crude glycerol by Bacillus sphaericus NII 0838 and improving its thermal properties by blending with other polymers Sindhu, Raveendran; Ammu, Balakrishnan; Binod, Parameswaran Brazilian Archives of Biology and Technology, Vol. 54, Issue 4 https://doi.org/10.1590/S1516-89132011000400019	journal	August 2011
Biofilm-specific antibiotic resistance Mah, Thien-Fah Future Microbiology, Vol. 7, Issue 9 https://doi.org/10.2217/fmb.12.76	journal	September 2012
Biofilms: Microbial Life on Surfaces Donlan, Rodney M. Emerging Infectious Diseases, Vol. 8, Issue 9 https://doi.org/10.3201/eid0809.020063	journal	September 2002
Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth Beckwith, Christopher R.; Edwards, Marcus J.; Lawes, Matthew Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00332	journal	April 2015
Direct involvement of ombB, omaB, and omcB genes in extracellular reduction of Fe(III) by Geobacter sulfurreducens PCA Liu, Yimo; Fredrickson, James K.; Zachara, John M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01075	journal	October 2015
The Low Conductivity of Geobacter uraniireducens Pili Suggests a Diversity of Extracellular Electron Transfer Mechanisms in the Genus Geobacter Tan, Yang; Adhikari, Ramesh Y.; Malvankar, Nikhil S. Frontiers in Microbiology, Vol. 07 https://doi.org/10.3389/fmicb.2016.00980	journal	June 2016
Extracellular Electron Transfer via Outer Membrane Cytochromes in a Methanotrophic Bacterium Methylococcus capsulatus (Bath) Tanaka, Kenya; Yokoe, Sho; Igarashi, Kensuke Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02905	journal	November 2018
Electroactive Bacteria Associated With Stainless Steel Ennoblement in Seawater Trigodet, Florian; Larché, Nicolas; Morrison, Hilary G. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00170	journal	February 2019
Discovery and Therapeutic Targeting of Differentiated Biofilm Subpopulations Bisht, Karishma; Wakeman, Catherine Ann Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01908	journal	August 2019
Geobacter Protein Nanowires Lovley, Derek R.; Walker, David J. F. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02078	journal	September 2019
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On the Edge of Research and Technological Application: A Critical Review of Electromethanogenesis Blasco-Gómez, Ramiro; Batlle-Vilanova, Pau; Villano, Marianna International Journal of Molecular Sciences, Vol. 18, Issue 4 https://doi.org/10.3390/ijms18040874	journal	April 2017
Improving the Cathodic Biofilm Growth Capabilities of Kyrpidia spormannii EA-1 by Undirected Mutagenesis Jung, Tobias; Hackbarth, Max; Horn, Harald Microorganisms, Vol. 9, Issue 1 https://doi.org/10.3390/microorganisms9010077	journal	December 2020
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Production of Polyhydroxybutyrate (PHB) and Factors Impacting Its Chemical and Mechanical Characteristics McAdam, Blaithín; Brennan Fournet, Margaret; McDonald, Paul Polymers, Vol. 12, Issue 12 https://doi.org/10.3390/polym12122908	journal	December 2020

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