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The root zone of graminoids: A niche for H(2)-consuming acetogens in a minerotrophic peatland
The importance of acetogens for H(2) turnover and overall anaerobic degradation in peatlands remains elusive. In the well-studied minerotrophic peatland fen Schlöppnerbrunnen, H(2)-consuming acetogens are conceptualized to be largely outcompeted by iron reducers, sulfate reducers, and hydrogenotroph...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9391049/ https://www.ncbi.nlm.nih.gov/pubmed/35992704 http://dx.doi.org/10.3389/fmicb.2022.978296 |
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author | Meier, Anja B. Oppermann, Sindy Drake, Harold L. Schmidt, Oliver |
author_facet | Meier, Anja B. Oppermann, Sindy Drake, Harold L. Schmidt, Oliver |
author_sort | Meier, Anja B. |
collection | PubMed |
description | The importance of acetogens for H(2) turnover and overall anaerobic degradation in peatlands remains elusive. In the well-studied minerotrophic peatland fen Schlöppnerbrunnen, H(2)-consuming acetogens are conceptualized to be largely outcompeted by iron reducers, sulfate reducers, and hydrogenotrophic methanogens in bulk peat soil. However, in root zones of graminoids, fermenters thriving on rhizodeposits and root litter might temporarily provide sufficient H(2) for acetogens. In the present study, root-free peat soils from around the roots of Molinia caerulea and Carex rostrata (i.e., two graminoids common in fen Schlöpnnerbrunnen) were anoxically incubated with or without supplemental H(2) to simulate conditions of high and low H(2) availability in the fen. In unsupplemented soil treatments, H(2) concentrations were largely below the detection limit (∼10 ppmV) and possibly too low for acetogens and methanogens, an assumption supported by the finding that neither acetate nor methane substantially accumulated. In the presence of supplemental H(2), acetate accumulation exceeded CH(4) accumulation in Molinia soil whereas acetate and methane accumulated equally in Carex soil. However, reductant recoveries indicated that initially, additional unknown processes were involved either in H(2) consumption or the consumption of acetate produced by H(2)-consuming acetogens. 16S rRNA and 16S rRNA gene analyses revealed that potential acetogens (Clostridium, Holophagaceae), methanogens (Methanocellales, Methanobacterium), iron reducers (Geobacter), and physiologically uncharacterized phylotypes (Acidobacteria, Actinobacteria, Bacteroidetes) were stimulated by supplemental H(2) in soil treatments. Phylotypes closely related to clostridial acetogens were also active in soil-free Molinia and Carex root treatments with or without supplemental H(2). Due to pronounced fermentation activities, H(2) consumption was less obvious in root treatments, and acetogens likely thrived on root organic carbon and fermentation products (e.g., ethanol) in addition to H(2). Collectively, the data highlighted that in fen Schlöppnerbrunnen, acetogens are associated to graminoid roots and inhabit the peat soil around the roots, where they have to compete for H(2) with methanogens and iron reducers. Furthermore, the study underscored that the metabolically flexible acetogens do not rely on H(2), potentially a key advantage over other H(2) consumers under the highly dynamic conditions characteristic for the root-zones of graminoids in peatlands. |
format | Online Article Text |
id | pubmed-9391049 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-93910492022-08-20 The root zone of graminoids: A niche for H(2)-consuming acetogens in a minerotrophic peatland Meier, Anja B. Oppermann, Sindy Drake, Harold L. Schmidt, Oliver Front Microbiol Microbiology The importance of acetogens for H(2) turnover and overall anaerobic degradation in peatlands remains elusive. In the well-studied minerotrophic peatland fen Schlöppnerbrunnen, H(2)-consuming acetogens are conceptualized to be largely outcompeted by iron reducers, sulfate reducers, and hydrogenotrophic methanogens in bulk peat soil. However, in root zones of graminoids, fermenters thriving on rhizodeposits and root litter might temporarily provide sufficient H(2) for acetogens. In the present study, root-free peat soils from around the roots of Molinia caerulea and Carex rostrata (i.e., two graminoids common in fen Schlöpnnerbrunnen) were anoxically incubated with or without supplemental H(2) to simulate conditions of high and low H(2) availability in the fen. In unsupplemented soil treatments, H(2) concentrations were largely below the detection limit (∼10 ppmV) and possibly too low for acetogens and methanogens, an assumption supported by the finding that neither acetate nor methane substantially accumulated. In the presence of supplemental H(2), acetate accumulation exceeded CH(4) accumulation in Molinia soil whereas acetate and methane accumulated equally in Carex soil. However, reductant recoveries indicated that initially, additional unknown processes were involved either in H(2) consumption or the consumption of acetate produced by H(2)-consuming acetogens. 16S rRNA and 16S rRNA gene analyses revealed that potential acetogens (Clostridium, Holophagaceae), methanogens (Methanocellales, Methanobacterium), iron reducers (Geobacter), and physiologically uncharacterized phylotypes (Acidobacteria, Actinobacteria, Bacteroidetes) were stimulated by supplemental H(2) in soil treatments. Phylotypes closely related to clostridial acetogens were also active in soil-free Molinia and Carex root treatments with or without supplemental H(2). Due to pronounced fermentation activities, H(2) consumption was less obvious in root treatments, and acetogens likely thrived on root organic carbon and fermentation products (e.g., ethanol) in addition to H(2). Collectively, the data highlighted that in fen Schlöppnerbrunnen, acetogens are associated to graminoid roots and inhabit the peat soil around the roots, where they have to compete for H(2) with methanogens and iron reducers. Furthermore, the study underscored that the metabolically flexible acetogens do not rely on H(2), potentially a key advantage over other H(2) consumers under the highly dynamic conditions characteristic for the root-zones of graminoids in peatlands. Frontiers Media S.A. 2022-08-05 /pmc/articles/PMC9391049/ /pubmed/35992704 http://dx.doi.org/10.3389/fmicb.2022.978296 Text en Copyright © 2022 Meier, Oppermann, Drake and Schmidt. https://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 Meier, Anja B. Oppermann, Sindy Drake, Harold L. Schmidt, Oliver The root zone of graminoids: A niche for H(2)-consuming acetogens in a minerotrophic peatland |
title | The root zone of graminoids: A niche for H(2)-consuming acetogens in a minerotrophic peatland |
title_full | The root zone of graminoids: A niche for H(2)-consuming acetogens in a minerotrophic peatland |
title_fullStr | The root zone of graminoids: A niche for H(2)-consuming acetogens in a minerotrophic peatland |
title_full_unstemmed | The root zone of graminoids: A niche for H(2)-consuming acetogens in a minerotrophic peatland |
title_short | The root zone of graminoids: A niche for H(2)-consuming acetogens in a minerotrophic peatland |
title_sort | root zone of graminoids: a niche for h(2)-consuming acetogens in a minerotrophic peatland |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9391049/ https://www.ncbi.nlm.nih.gov/pubmed/35992704 http://dx.doi.org/10.3389/fmicb.2022.978296 |
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