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Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus

Extracellular electron transfer (EET), the process that allows microbes to exchange electrons in a redox capacity with solid interfaces such as minerals or electrodes, has been predominantly described in microbes that use iron during respiration. In this work, we characterize the physiology, genome,...

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Autores principales: Vinales, Jorge, Sackett, Joshua, Trutschel, Leah, Amir, Waleed, Norman, Casey, Leach, Edmund, Wilbanks, Elizabeth, Rowe, Annette
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9230427/
https://www.ncbi.nlm.nih.gov/pubmed/35744737
http://dx.doi.org/10.3390/microorganisms10061219
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author Vinales, Jorge
Sackett, Joshua
Trutschel, Leah
Amir, Waleed
Norman, Casey
Leach, Edmund
Wilbanks, Elizabeth
Rowe, Annette
author_facet Vinales, Jorge
Sackett, Joshua
Trutschel, Leah
Amir, Waleed
Norman, Casey
Leach, Edmund
Wilbanks, Elizabeth
Rowe, Annette
author_sort Vinales, Jorge
collection PubMed
description Extracellular electron transfer (EET), the process that allows microbes to exchange electrons in a redox capacity with solid interfaces such as minerals or electrodes, has been predominantly described in microbes that use iron during respiration. In this work, we characterize the physiology, genome, and electrochemical properties of two obligately heterotrophic marine microbes that were previously isolated from marine sediment cathode enrichments. Phylogenetic analysis of isolate 16S rRNA genes showed two strains, SN11 and FeN1, belonging to the genus Idiomarina. Strain SN11 was found to be nearly identical to I. loihiensis L2-TR(T), and strain FeN1 was most closely related to I. maritima 908087(T). Each strain had a relatively small genome (~2.8–2.9 MB). Phenotypic similarities among FeN1, SN11, and the studied strains include being Gram-negative, motile, catalase- and oxidase-positive, and rod-shaped. Physiologically, all strains appeared to exclusively use amino acids as a primary carbon source for growth. This was consistent with genomic observations. Each strain contained 17 to 22 proteins with heme-binding motifs. None of these were predicted to be extracellular, although seven were of unknown localization and lacked functional annotation beyond cytochrome. Despite the lack of homology to known EET pathways, both FeN1 and SN11 were capable of sustained electron uptake over time in an electrochemical system linked to respiration. Given the association of these Idiomarina strains with electro-active biofilms in the environment and their lack of autotrophic capabilities, we predict that EET is used exclusively for respiration in these microbes.
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spelling pubmed-92304272022-06-25 Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus Vinales, Jorge Sackett, Joshua Trutschel, Leah Amir, Waleed Norman, Casey Leach, Edmund Wilbanks, Elizabeth Rowe, Annette Microorganisms Article Extracellular electron transfer (EET), the process that allows microbes to exchange electrons in a redox capacity with solid interfaces such as minerals or electrodes, has been predominantly described in microbes that use iron during respiration. In this work, we characterize the physiology, genome, and electrochemical properties of two obligately heterotrophic marine microbes that were previously isolated from marine sediment cathode enrichments. Phylogenetic analysis of isolate 16S rRNA genes showed two strains, SN11 and FeN1, belonging to the genus Idiomarina. Strain SN11 was found to be nearly identical to I. loihiensis L2-TR(T), and strain FeN1 was most closely related to I. maritima 908087(T). Each strain had a relatively small genome (~2.8–2.9 MB). Phenotypic similarities among FeN1, SN11, and the studied strains include being Gram-negative, motile, catalase- and oxidase-positive, and rod-shaped. Physiologically, all strains appeared to exclusively use amino acids as a primary carbon source for growth. This was consistent with genomic observations. Each strain contained 17 to 22 proteins with heme-binding motifs. None of these were predicted to be extracellular, although seven were of unknown localization and lacked functional annotation beyond cytochrome. Despite the lack of homology to known EET pathways, both FeN1 and SN11 were capable of sustained electron uptake over time in an electrochemical system linked to respiration. Given the association of these Idiomarina strains with electro-active biofilms in the environment and their lack of autotrophic capabilities, we predict that EET is used exclusively for respiration in these microbes. MDPI 2022-06-14 /pmc/articles/PMC9230427/ /pubmed/35744737 http://dx.doi.org/10.3390/microorganisms10061219 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Vinales, Jorge
Sackett, Joshua
Trutschel, Leah
Amir, Waleed
Norman, Casey
Leach, Edmund
Wilbanks, Elizabeth
Rowe, Annette
Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus
title Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus
title_full Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus
title_fullStr Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus
title_full_unstemmed Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus
title_short Physiologic, Genomic, and Electrochemical Characterization of Two Heterotrophic Marine Sediment Microbes from the Idiomarina Genus
title_sort physiologic, genomic, and electrochemical characterization of two heterotrophic marine sediment microbes from the idiomarina genus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9230427/
https://www.ncbi.nlm.nih.gov/pubmed/35744737
http://dx.doi.org/10.3390/microorganisms10061219
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