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Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey

Terrestrial hydrothermal springs and aquifers are excellent sites to study microbial biogeography because of their high physicochemical heterogeneity across relatively limited geographic regions. In this study, we performed 16S rRNA gene sequencing and metagenomic analyses of the microbial diversity...

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Autores principales: Coskun, Ömer K., Gomez-Saez, Gonzalo V., Beren, Murat, Ozcan, Dogacan, Hosgormez, Hakan, Einsiedl, Florian, Orsi, William D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9992828/
https://www.ncbi.nlm.nih.gov/pubmed/36910224
http://dx.doi.org/10.3389/fmicb.2023.1063139
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author Coskun, Ömer K.
Gomez-Saez, Gonzalo V.
Beren, Murat
Ozcan, Dogacan
Hosgormez, Hakan
Einsiedl, Florian
Orsi, William D.
author_facet Coskun, Ömer K.
Gomez-Saez, Gonzalo V.
Beren, Murat
Ozcan, Dogacan
Hosgormez, Hakan
Einsiedl, Florian
Orsi, William D.
author_sort Coskun, Ömer K.
collection PubMed
description Terrestrial hydrothermal springs and aquifers are excellent sites to study microbial biogeography because of their high physicochemical heterogeneity across relatively limited geographic regions. In this study, we performed 16S rRNA gene sequencing and metagenomic analyses of the microbial diversity of 11 different geothermal aquifers and springs across the tectonically active Biga Peninsula (Turkey). Across geothermal settings ranging in temperature from 43 to 79°C, one of the most highly represented groups in both 16S rRNA gene and metagenomic datasets was affiliated with the uncultivated phylum “Candidatus Bipolaricaulota” (former “Ca. Acetothermia” and OP1 division). The highest relative abundance of “Ca. Bipolaricaulota” was observed in a 68°C geothermal brine sediment, where it dominated the microbial community, representing 91% of all detectable 16S rRNA genes. Correlation analysis of “Ca. Bipolaricaulota” operational taxonomic units (OTUs) with physicochemical parameters indicated that salinity was the strongest environmental factor measured associated with the distribution of this novel group in geothermal fluids. Correspondingly, analysis of 23 metagenome-assembled genomes (MAGs) revealed two distinct groups of “Ca. Bipolaricaulota” MAGs based on the differences in carbon metabolism: one group encoding the bacterial Wood-Ljungdahl pathway (WLP) for H(2) dependent CO(2) fixation is selected for at lower salinities, and a second heterotrophic clade that lacks the WLP that was selected for under hypersaline conditions in the geothermal brine sediment. In conclusion, our results highlight that the biogeography of “Ca. Bipolaricaulota” taxa is strongly correlated with salinity in hydrothermal ecosystems, which coincides with key differences in carbon acquisition strategies. The exceptionally high relative abundance of apparently heterotrophic representatives of this novel candidate Phylum in geothermal brine sediment observed here may help to guide future enrichment experiments to obtain representatives in pure culture.
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spelling pubmed-99928282023-03-09 Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey Coskun, Ömer K. Gomez-Saez, Gonzalo V. Beren, Murat Ozcan, Dogacan Hosgormez, Hakan Einsiedl, Florian Orsi, William D. Front Microbiol Microbiology Terrestrial hydrothermal springs and aquifers are excellent sites to study microbial biogeography because of their high physicochemical heterogeneity across relatively limited geographic regions. In this study, we performed 16S rRNA gene sequencing and metagenomic analyses of the microbial diversity of 11 different geothermal aquifers and springs across the tectonically active Biga Peninsula (Turkey). Across geothermal settings ranging in temperature from 43 to 79°C, one of the most highly represented groups in both 16S rRNA gene and metagenomic datasets was affiliated with the uncultivated phylum “Candidatus Bipolaricaulota” (former “Ca. Acetothermia” and OP1 division). The highest relative abundance of “Ca. Bipolaricaulota” was observed in a 68°C geothermal brine sediment, where it dominated the microbial community, representing 91% of all detectable 16S rRNA genes. Correlation analysis of “Ca. Bipolaricaulota” operational taxonomic units (OTUs) with physicochemical parameters indicated that salinity was the strongest environmental factor measured associated with the distribution of this novel group in geothermal fluids. Correspondingly, analysis of 23 metagenome-assembled genomes (MAGs) revealed two distinct groups of “Ca. Bipolaricaulota” MAGs based on the differences in carbon metabolism: one group encoding the bacterial Wood-Ljungdahl pathway (WLP) for H(2) dependent CO(2) fixation is selected for at lower salinities, and a second heterotrophic clade that lacks the WLP that was selected for under hypersaline conditions in the geothermal brine sediment. In conclusion, our results highlight that the biogeography of “Ca. Bipolaricaulota” taxa is strongly correlated with salinity in hydrothermal ecosystems, which coincides with key differences in carbon acquisition strategies. The exceptionally high relative abundance of apparently heterotrophic representatives of this novel candidate Phylum in geothermal brine sediment observed here may help to guide future enrichment experiments to obtain representatives in pure culture. Frontiers Media S.A. 2023-02-22 /pmc/articles/PMC9992828/ /pubmed/36910224 http://dx.doi.org/10.3389/fmicb.2023.1063139 Text en Copyright © 2023 Coskun, Gomez-Saez, Beren, Ozcan, Hosgormez, Einsiedl and Orsi. 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
Coskun, Ömer K.
Gomez-Saez, Gonzalo V.
Beren, Murat
Ozcan, Dogacan
Hosgormez, Hakan
Einsiedl, Florian
Orsi, William D.
Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey
title Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey
title_full Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey
title_fullStr Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey
title_full_unstemmed Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey
title_short Carbon metabolism and biogeography of candidate phylum “Candidatus Bipolaricaulota” in geothermal environments of Biga Peninsula, Turkey
title_sort carbon metabolism and biogeography of candidate phylum “candidatus bipolaricaulota” in geothermal environments of biga peninsula, turkey
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9992828/
https://www.ncbi.nlm.nih.gov/pubmed/36910224
http://dx.doi.org/10.3389/fmicb.2023.1063139
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