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Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H(2)S Production: Escherichia coli K-12 and Desulfovibrio sp. Strain DF1 as Co-culture Model

Sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) is produced by plants and other phototrophs and its biodegradation is a relevant component of the biogeochemical carbon and sulfur cycles. SQ is known to be degraded by aerobic bacterial consortia in two tiers via C(3)-organosulfonates as transient interme...

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Autores principales: Burrichter, Anna, Denger, Karin, Franchini, Paolo, Huhn, Thomas, Müller, Nicolai, Spiteller, Dieter, Schleheck, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6278857/
https://www.ncbi.nlm.nih.gov/pubmed/30546350
http://dx.doi.org/10.3389/fmicb.2018.02792
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author Burrichter, Anna
Denger, Karin
Franchini, Paolo
Huhn, Thomas
Müller, Nicolai
Spiteller, Dieter
Schleheck, David
author_facet Burrichter, Anna
Denger, Karin
Franchini, Paolo
Huhn, Thomas
Müller, Nicolai
Spiteller, Dieter
Schleheck, David
author_sort Burrichter, Anna
collection PubMed
description Sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) is produced by plants and other phototrophs and its biodegradation is a relevant component of the biogeochemical carbon and sulfur cycles. SQ is known to be degraded by aerobic bacterial consortia in two tiers via C(3)-organosulfonates as transient intermediates to CO(2), water and sulfate. In this study, we present a first laboratory model for anaerobic degradation of SQ by bacterial consortia in two tiers to acetate and hydrogen sulfide (H(2)S). For the first tier, SQ-degrading Escherichia coli K-12 was used. It catalyzes the fermentation of SQ to 2,3-dihydroxypropane-1-sulfonate (DHPS), succinate, acetate and formate, thus, a novel type of mixed-acid fermentation. It employs the characterized SQ Embden-Meyerhof-Parnas pathway, as confirmed by mutational and proteomic analyses. For the second tier, a DHPS-degrading Desulfovibrio sp. isolate from anaerobic sewage sludge was used, strain DF1. It catalyzes another novel fermentation, of the DHPS to acetate and H(2)S. Its DHPS desulfonation pathway was identified by differential proteomics and demonstrated by heterologously produced enzymes: DHPS is oxidized via 3-sulfolactaldehyde to 3-sulfolactate (SL) by two NAD(+)-dependent dehydrogenases (DhpA, SlaB); the SL is cleaved by an SL sulfite-lyase known from aerobic bacteria (SuyAB) to pyruvate and sulfite. The pyruvate is oxidized to acetate, while the sulfite is used as electron acceptor in respiration and reduced to H(2)S. In conclusion, anaerobic sulfidogenic SQ degradation was demonstrated as a novel link in the biogeochemical sulfur cycle. SQ is also a constituent of the green-vegetable diet of herbivores and omnivores and H(2)S production in the intestinal microbiome has many recognized and potential contributions to human health and disease. Hence, it is important to examine bacterial SQ degradation also in the human intestinal microbiome, in relation to H(2)S production, dietary conditions and human health.
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spelling pubmed-62788572018-12-13 Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H(2)S Production: Escherichia coli K-12 and Desulfovibrio sp. Strain DF1 as Co-culture Model Burrichter, Anna Denger, Karin Franchini, Paolo Huhn, Thomas Müller, Nicolai Spiteller, Dieter Schleheck, David Front Microbiol Microbiology Sulfoquinovose (SQ, 6-deoxy-6-sulfoglucose) is produced by plants and other phototrophs and its biodegradation is a relevant component of the biogeochemical carbon and sulfur cycles. SQ is known to be degraded by aerobic bacterial consortia in two tiers via C(3)-organosulfonates as transient intermediates to CO(2), water and sulfate. In this study, we present a first laboratory model for anaerobic degradation of SQ by bacterial consortia in two tiers to acetate and hydrogen sulfide (H(2)S). For the first tier, SQ-degrading Escherichia coli K-12 was used. It catalyzes the fermentation of SQ to 2,3-dihydroxypropane-1-sulfonate (DHPS), succinate, acetate and formate, thus, a novel type of mixed-acid fermentation. It employs the characterized SQ Embden-Meyerhof-Parnas pathway, as confirmed by mutational and proteomic analyses. For the second tier, a DHPS-degrading Desulfovibrio sp. isolate from anaerobic sewage sludge was used, strain DF1. It catalyzes another novel fermentation, of the DHPS to acetate and H(2)S. Its DHPS desulfonation pathway was identified by differential proteomics and demonstrated by heterologously produced enzymes: DHPS is oxidized via 3-sulfolactaldehyde to 3-sulfolactate (SL) by two NAD(+)-dependent dehydrogenases (DhpA, SlaB); the SL is cleaved by an SL sulfite-lyase known from aerobic bacteria (SuyAB) to pyruvate and sulfite. The pyruvate is oxidized to acetate, while the sulfite is used as electron acceptor in respiration and reduced to H(2)S. In conclusion, anaerobic sulfidogenic SQ degradation was demonstrated as a novel link in the biogeochemical sulfur cycle. SQ is also a constituent of the green-vegetable diet of herbivores and omnivores and H(2)S production in the intestinal microbiome has many recognized and potential contributions to human health and disease. Hence, it is important to examine bacterial SQ degradation also in the human intestinal microbiome, in relation to H(2)S production, dietary conditions and human health. Frontiers Media S.A. 2018-11-27 /pmc/articles/PMC6278857/ /pubmed/30546350 http://dx.doi.org/10.3389/fmicb.2018.02792 Text en Copyright © 2018 Burrichter, Denger, Franchini, Huhn, Müller, Spiteller and Schleheck. 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 Microbiology
Burrichter, Anna
Denger, Karin
Franchini, Paolo
Huhn, Thomas
Müller, Nicolai
Spiteller, Dieter
Schleheck, David
Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H(2)S Production: Escherichia coli K-12 and Desulfovibrio sp. Strain DF1 as Co-culture Model
title Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H(2)S Production: Escherichia coli K-12 and Desulfovibrio sp. Strain DF1 as Co-culture Model
title_full Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H(2)S Production: Escherichia coli K-12 and Desulfovibrio sp. Strain DF1 as Co-culture Model
title_fullStr Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H(2)S Production: Escherichia coli K-12 and Desulfovibrio sp. Strain DF1 as Co-culture Model
title_full_unstemmed Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H(2)S Production: Escherichia coli K-12 and Desulfovibrio sp. Strain DF1 as Co-culture Model
title_short Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H(2)S Production: Escherichia coli K-12 and Desulfovibrio sp. Strain DF1 as Co-culture Model
title_sort anaerobic degradation of the plant sugar sulfoquinovose concomitant with h(2)s production: escherichia coli k-12 and desulfovibrio sp. strain df1 as co-culture model
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6278857/
https://www.ncbi.nlm.nih.gov/pubmed/30546350
http://dx.doi.org/10.3389/fmicb.2018.02792
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