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Sulfate Alters the Competition Among Microbiome Members of Sediments Chronically Exposed to Asphalt

Sulfate-reducing microorganisms (SRMs) often compete with methanogens for common substrates. Due to thermodynamic reasons, SRMs should outcompete methanogens in the presence of sulfate. However, many studies have documented coexistence of these microbial groups in natural environments, suggesting th...

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Autores principales: Michas, Antonios, Harir, Mourad, Lucio, Marianna, Vestergaard, Gisle, Himmelberg, Anne, Schmitt-Kopplin, Philippe, Lueders, Tillmann, Hatzinikolaou, Dimitris G., Schöler, Anne, Rabus, Ralf, Schloter, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7550536/
https://www.ncbi.nlm.nih.gov/pubmed/33133031
http://dx.doi.org/10.3389/fmicb.2020.556793
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author Michas, Antonios
Harir, Mourad
Lucio, Marianna
Vestergaard, Gisle
Himmelberg, Anne
Schmitt-Kopplin, Philippe
Lueders, Tillmann
Hatzinikolaou, Dimitris G.
Schöler, Anne
Rabus, Ralf
Schloter, Michael
author_facet Michas, Antonios
Harir, Mourad
Lucio, Marianna
Vestergaard, Gisle
Himmelberg, Anne
Schmitt-Kopplin, Philippe
Lueders, Tillmann
Hatzinikolaou, Dimitris G.
Schöler, Anne
Rabus, Ralf
Schloter, Michael
author_sort Michas, Antonios
collection PubMed
description Sulfate-reducing microorganisms (SRMs) often compete with methanogens for common substrates. Due to thermodynamic reasons, SRMs should outcompete methanogens in the presence of sulfate. However, many studies have documented coexistence of these microbial groups in natural environments, suggesting that thermodynamics alone cannot explain the interactions among them. In this study, we investigated how SRMs compete with the established methanogenic communities in sediment from a long-term, electron acceptor-depleted, asphalt-exposed ecosystem and how they affect the composition of the organic material. We hypothesized that, upon addition of sulfate, SRMs (i) outcompete the methanogenic communities and (ii) markedly contribute to transformations of the organic material. We sampled sediments from the test and proximate control sites under anoxic conditions and incubated them in seawater medium with or without sulfate. Abundance and activity pattern of SRMs and methanogens, as well as the total prokaryotic community, were followed for 6 weeks by using qPCR targeting selected marker genes. Some of these genes were also subjected to amplicon sequencing to assess potential shifts in diversity patterns. Alterations of the organic material in the microcosms were determined by mass spectrometry. Our results indicate that the competition of SRMs with methanogens upon sulfate addition strongly depends on the environment studied and the starting microbiome composition. In the asphalt-free sediments (control), the availability of easily degradable organic material (mainly plant-derived) allows SRMs to use a larger variety of substrates, reducing interspecies competition with methanogens. In contrast, the abundant presence of recalcitrant compounds in the asphalt-exposed sediment was associated with a strong competition between SRMs and methanogens, ultimately detrimental for the latter. Our data underpin the importance of the quality of bioavailable organic materials in anoxic environments as a driver for microbial community structure and function.
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spelling pubmed-75505362020-10-29 Sulfate Alters the Competition Among Microbiome Members of Sediments Chronically Exposed to Asphalt Michas, Antonios Harir, Mourad Lucio, Marianna Vestergaard, Gisle Himmelberg, Anne Schmitt-Kopplin, Philippe Lueders, Tillmann Hatzinikolaou, Dimitris G. Schöler, Anne Rabus, Ralf Schloter, Michael Front Microbiol Microbiology Sulfate-reducing microorganisms (SRMs) often compete with methanogens for common substrates. Due to thermodynamic reasons, SRMs should outcompete methanogens in the presence of sulfate. However, many studies have documented coexistence of these microbial groups in natural environments, suggesting that thermodynamics alone cannot explain the interactions among them. In this study, we investigated how SRMs compete with the established methanogenic communities in sediment from a long-term, electron acceptor-depleted, asphalt-exposed ecosystem and how they affect the composition of the organic material. We hypothesized that, upon addition of sulfate, SRMs (i) outcompete the methanogenic communities and (ii) markedly contribute to transformations of the organic material. We sampled sediments from the test and proximate control sites under anoxic conditions and incubated them in seawater medium with or without sulfate. Abundance and activity pattern of SRMs and methanogens, as well as the total prokaryotic community, were followed for 6 weeks by using qPCR targeting selected marker genes. Some of these genes were also subjected to amplicon sequencing to assess potential shifts in diversity patterns. Alterations of the organic material in the microcosms were determined by mass spectrometry. Our results indicate that the competition of SRMs with methanogens upon sulfate addition strongly depends on the environment studied and the starting microbiome composition. In the asphalt-free sediments (control), the availability of easily degradable organic material (mainly plant-derived) allows SRMs to use a larger variety of substrates, reducing interspecies competition with methanogens. In contrast, the abundant presence of recalcitrant compounds in the asphalt-exposed sediment was associated with a strong competition between SRMs and methanogens, ultimately detrimental for the latter. Our data underpin the importance of the quality of bioavailable organic materials in anoxic environments as a driver for microbial community structure and function. Frontiers Media S.A. 2020-09-29 /pmc/articles/PMC7550536/ /pubmed/33133031 http://dx.doi.org/10.3389/fmicb.2020.556793 Text en Copyright © 2020 Michas, Harir, Lucio, Vestergaard, Himmelberg, Schmitt-Kopplin, Lueders, Hatzinikolaou, Schöler, Rabus and Schloter. 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
Michas, Antonios
Harir, Mourad
Lucio, Marianna
Vestergaard, Gisle
Himmelberg, Anne
Schmitt-Kopplin, Philippe
Lueders, Tillmann
Hatzinikolaou, Dimitris G.
Schöler, Anne
Rabus, Ralf
Schloter, Michael
Sulfate Alters the Competition Among Microbiome Members of Sediments Chronically Exposed to Asphalt
title Sulfate Alters the Competition Among Microbiome Members of Sediments Chronically Exposed to Asphalt
title_full Sulfate Alters the Competition Among Microbiome Members of Sediments Chronically Exposed to Asphalt
title_fullStr Sulfate Alters the Competition Among Microbiome Members of Sediments Chronically Exposed to Asphalt
title_full_unstemmed Sulfate Alters the Competition Among Microbiome Members of Sediments Chronically Exposed to Asphalt
title_short Sulfate Alters the Competition Among Microbiome Members of Sediments Chronically Exposed to Asphalt
title_sort sulfate alters the competition among microbiome members of sediments chronically exposed to asphalt
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7550536/
https://www.ncbi.nlm.nih.gov/pubmed/33133031
http://dx.doi.org/10.3389/fmicb.2020.556793
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