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Evidence of a Streamlined Extracellular Electron Transfer Pathway from Biofilm Structure, Metabolic Stratification, and Long-Range Electron Transfer Parameters

Jiménez Otero, Fernanda and Chadwick, Grayson L. and Yates, Matthew D. and Mickol, Rebecca L. and Saunders, Scott H. and Glaven, Sarah M. and Gralnick, Jeffrey A. and Newman, Dianne K. and Tender, Leonard M. and Orphan, Victoria J. and Bond, Daniel R. (2021) Evidence of a Streamlined Extracellular Electron Transfer Pathway from Biofilm Structure, Metabolic Stratification, and Long-Range Electron Transfer Parameters. Applied and Environmental Microbiology, 87 (17). Art. No. AEM.00706-21. ISSN 0099-2240. PMCID PMC8357294. doi:10.1128/aem.00706-21.

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A strain of Geobacter sulfurreducens, an organism capable of respiring solid extracellular substrates, lacking four of five outer membrane cytochrome complexes (extABCD⁺ strain) grows faster and produces greater current density than the wild type grown under identical conditions. To understand cellular and biofilm modifications in the extABCD⁺ strain responsible for this increased performance, biofilms grown using electrodes as terminal electron acceptors were sectioned and imaged using electron microscopy to determine changes in thickness and cell density, while parallel biofilms incubated in the presence of nitrogen and carbon isotopes were analyzed using NanoSIMS (nanoscale secondary ion mass spectrometry) to quantify and localize anabolic activity. Long-distance electron transfer parameters were measured for wild-type and extABCD⁺ biofilms spanning 5-μm gaps. Our results reveal that extABCD⁺ biofilms achieved higher current densities through the additive effects of denser cell packing close to the electrode (based on electron microscopy), combined with higher metabolic rates per cell compared to the wild type (based on increased rates of ¹⁵N incorporation). We also observed an increased rate of electron transfer through extABCD⁺ versus wild-type biofilms, suggesting that denser biofilms resulting from the deletion of unnecessary multiheme cytochromes streamline electron transfer to electrodes. The combination of imaging, physiological, and electrochemical data confirms that engineered electrogenic bacteria are capable of producing more current per cell and, in combination with higher biofilm density and electron diffusion rates, can produce a higher final current density than the wild type.

Item Type:Article
Related URLs:
URLURL TypeDescription CentralArticle
Jiménez Otero, Fernanda0000-0003-1583-6495
Chadwick, Grayson L.0000-0003-0700-9350
Yates, Matthew D.0000-0003-4373-3864
Mickol, Rebecca L.0000-0002-4493-7263
Saunders, Scott H.0000-0003-4224-9106
Glaven, Sarah M.0000-0003-0857-3391
Gralnick, Jeffrey A.0000-0001-9250-7770
Newman, Dianne K.0000-0003-1647-1918
Tender, Leonard M.0000-0001-8784-991X
Orphan, Victoria J.0000-0002-5374-6178
Bond, Daniel R.0000-0001-8083-7107
Additional Information:© 2021 Jiménez Otero et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 12 April 2021; Accepted 15 June 2021; Accepted manuscript posted online 30 June 2021; Published 11 August 2021. This research was supported by the Office of Naval Research (N00014-18-1-2632) to D.R.B., a grant from the Simons Foundation collaboration on Principles of Microbial Ecosystems (PriME) to V.J.O., and the National Institutes of Health (1R01AI127850-01A1) to D.K.N. F.J.O. was supported by the National Council of Science and Technology of Mexico (CONACYT).
Funding AgencyGrant Number
Office of Naval Research (ONR)N00014-18-1-2632
Simons FoundationUNSPECIFIED
Consejo Nacional de Ciencia y Tecnología (CONACYT)UNSPECIFIED
Issue or Number:17
PubMed Central ID:PMC8357294
Record Number:CaltechAUTHORS:20210714-151655967
Persistent URL:
Official Citation:Jiménez Otero F, Chadwick GL, Yates MD, Mickol RL, Saunders SH, Glaven SM, Gralnick JA, Newman DK, Tender LM, Orphan VJ, Bond DR. 2021. Evidence of a streamlined extracellular electron transfer pathway from biofilm structure, metabolic stratification, and long-range electron transfer parameters. Appl Environ Microbiol 87:e00706-21.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:109805
Deposited By: Tony Diaz
Deposited On:14 Jul 2021 18:17
Last Modified:02 Feb 2022 18:48

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