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Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis

Electroautotrophy is a novel and fascinating microbial metabolism, with tremendous potential for CO(2) storage and valorization into chemicals and materials made thereof. Research attention has been devoted toward the characterization of acetogenic and methanogenic electroautotrophs. In contrast, he...

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Autores principales: Agostino, Valeria, Lenic, Annika, Bardl, Bettina, Rizzotto, Valentina, Phan, An N. T., Blank, Lars M., Rosenbaum, Miriam A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7248197/
https://www.ncbi.nlm.nih.gov/pubmed/32509745
http://dx.doi.org/10.3389/fbioe.2020.00457
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author Agostino, Valeria
Lenic, Annika
Bardl, Bettina
Rizzotto, Valentina
Phan, An N. T.
Blank, Lars M.
Rosenbaum, Miriam A.
author_facet Agostino, Valeria
Lenic, Annika
Bardl, Bettina
Rizzotto, Valentina
Phan, An N. T.
Blank, Lars M.
Rosenbaum, Miriam A.
author_sort Agostino, Valeria
collection PubMed
description Electroautotrophy is a novel and fascinating microbial metabolism, with tremendous potential for CO(2) storage and valorization into chemicals and materials made thereof. Research attention has been devoted toward the characterization of acetogenic and methanogenic electroautotrophs. In contrast, here we characterize the electrophysiology of a sulfate-reducing bacterium, Desulfosporosinus orientis, harboring the Wood-Ljungdahl pathway and, thus, capable of fixing CO(2) into acetyl-CoA. For most electroautotrophs the mode of electron uptake is still not fully clarified. Our electrochemical experiments at different polarization conditions and Fe(0) corrosion tests point to a H(2)- mediated electron uptake ability of this strain. This observation is in line with the lack of outer membrane and periplasmic multi-heme c-type cytochromes in this bacterium. Maximum planktonic biomass production and a maximum sulfate reduction rate of 2 ± 0.4 mM day(–1) were obtained with an applied cathode potential of −900 mV vs. Ag/AgCl, resulting in an electron recovery in sulfate reduction of 37 ± 1.4%. Anaerobic sulfate respiration is more thermodynamically favorable than acetogenesis. Nevertheless, D. orientis strains adapted to sulfate-limiting conditions, could be tuned to electrosynthetic production of up to 8 mM of acetate, which compares well with other electroacetogens. The yield per biomass was very similar to H(2)/CO(2) based acetogenesis. Acetate bioelectrosynthesis was confirmed through stable isotope labeling experiments with Na-H(13)CO(3). Our results highlight a great influence of the CO(2) feeding strategy and start-up H(2) level in the catholyte on planktonic biomass growth and acetate production. In serum bottles experiments, D. orientis also generated butyrate, which makes D. orientis even more attractive for bioelectrosynthesis application. A further optimization of these physiological pathways is needed to obtain electrosynthetic butyrate production in D. orientis biocathodes. This study expands the diversity of facultative autotrophs able to perform H(2)-mediated extracellular electron uptake in Bioelectrochemical Systems (BES). We characterized a sulfate-reducing and acetogenic bacterium, D. orientis, able to naturally produce acetate and butyrate from CO(2) and H(2). For any future bioprocess, the exploitation of planktonic growing electroautotrophs with H(2)-mediated electron uptake would allow for a better use of the entire liquid volume of the cathodic reactor and, thus, higher productivities and product yields from CO(2)-rich waste gas streams.
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spelling pubmed-72481972020-06-05 Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis Agostino, Valeria Lenic, Annika Bardl, Bettina Rizzotto, Valentina Phan, An N. T. Blank, Lars M. Rosenbaum, Miriam A. Front Bioeng Biotechnol Bioengineering and Biotechnology Electroautotrophy is a novel and fascinating microbial metabolism, with tremendous potential for CO(2) storage and valorization into chemicals and materials made thereof. Research attention has been devoted toward the characterization of acetogenic and methanogenic electroautotrophs. In contrast, here we characterize the electrophysiology of a sulfate-reducing bacterium, Desulfosporosinus orientis, harboring the Wood-Ljungdahl pathway and, thus, capable of fixing CO(2) into acetyl-CoA. For most electroautotrophs the mode of electron uptake is still not fully clarified. Our electrochemical experiments at different polarization conditions and Fe(0) corrosion tests point to a H(2)- mediated electron uptake ability of this strain. This observation is in line with the lack of outer membrane and periplasmic multi-heme c-type cytochromes in this bacterium. Maximum planktonic biomass production and a maximum sulfate reduction rate of 2 ± 0.4 mM day(–1) were obtained with an applied cathode potential of −900 mV vs. Ag/AgCl, resulting in an electron recovery in sulfate reduction of 37 ± 1.4%. Anaerobic sulfate respiration is more thermodynamically favorable than acetogenesis. Nevertheless, D. orientis strains adapted to sulfate-limiting conditions, could be tuned to electrosynthetic production of up to 8 mM of acetate, which compares well with other electroacetogens. The yield per biomass was very similar to H(2)/CO(2) based acetogenesis. Acetate bioelectrosynthesis was confirmed through stable isotope labeling experiments with Na-H(13)CO(3). Our results highlight a great influence of the CO(2) feeding strategy and start-up H(2) level in the catholyte on planktonic biomass growth and acetate production. In serum bottles experiments, D. orientis also generated butyrate, which makes D. orientis even more attractive for bioelectrosynthesis application. A further optimization of these physiological pathways is needed to obtain electrosynthetic butyrate production in D. orientis biocathodes. This study expands the diversity of facultative autotrophs able to perform H(2)-mediated extracellular electron uptake in Bioelectrochemical Systems (BES). We characterized a sulfate-reducing and acetogenic bacterium, D. orientis, able to naturally produce acetate and butyrate from CO(2) and H(2). For any future bioprocess, the exploitation of planktonic growing electroautotrophs with H(2)-mediated electron uptake would allow for a better use of the entire liquid volume of the cathodic reactor and, thus, higher productivities and product yields from CO(2)-rich waste gas streams. Frontiers Media S.A. 2020-05-19 /pmc/articles/PMC7248197/ /pubmed/32509745 http://dx.doi.org/10.3389/fbioe.2020.00457 Text en Copyright © 2020 Agostino, Lenic, Bardl, Rizzotto, Phan, Blank and Rosenbaum. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Bioengineering and Biotechnology
Agostino, Valeria
Lenic, Annika
Bardl, Bettina
Rizzotto, Valentina
Phan, An N. T.
Blank, Lars M.
Rosenbaum, Miriam A.
Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis
title Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis
title_full Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis
title_fullStr Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis
title_full_unstemmed Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis
title_short Electrophysiology of the Facultative Autotrophic Bacterium Desulfosporosinus orientis
title_sort electrophysiology of the facultative autotrophic bacterium desulfosporosinus orientis
topic Bioengineering and Biotechnology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7248197/
https://www.ncbi.nlm.nih.gov/pubmed/32509745
http://dx.doi.org/10.3389/fbioe.2020.00457
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