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A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments

BACKGROUND: Hypersaline soda lakes are characterized by extreme high soluble carbonate alkalinity. Despite the high pH and salt content, highly diverse microbial communities are known to be present in soda lake brines but the microbiome of soda lake sediments received much less attention of microbio...

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Autores principales: Vavourakis, Charlotte D., Andrei, Adrian-Stefan, Mehrshad, Maliheh, Ghai, Rohit, Sorokin, Dimitry Y., Muyzer, Gerard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6146748/
https://www.ncbi.nlm.nih.gov/pubmed/30231921
http://dx.doi.org/10.1186/s40168-018-0548-7
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author Vavourakis, Charlotte D.
Andrei, Adrian-Stefan
Mehrshad, Maliheh
Ghai, Rohit
Sorokin, Dimitry Y.
Muyzer, Gerard
author_facet Vavourakis, Charlotte D.
Andrei, Adrian-Stefan
Mehrshad, Maliheh
Ghai, Rohit
Sorokin, Dimitry Y.
Muyzer, Gerard
author_sort Vavourakis, Charlotte D.
collection PubMed
description BACKGROUND: Hypersaline soda lakes are characterized by extreme high soluble carbonate alkalinity. Despite the high pH and salt content, highly diverse microbial communities are known to be present in soda lake brines but the microbiome of soda lake sediments received much less attention of microbiologists. Here, we performed metagenomic sequencing on soda lake sediments to give the first extensive overview of the taxonomic diversity found in these complex, extreme environments and to gain novel physiological insights into the most abundant, uncultured prokaryote lineages. RESULTS: We sequenced five metagenomes obtained from four surface sediments of Siberian soda lakes with a pH 10 and a salt content between 70 and 400 g L(−1). The recovered 16S rRNA gene sequences were mostly from Bacteria, even in the salt-saturated lakes. Most OTUs were assigned to uncultured families. We reconstructed 871 metagenome-assembled genomes (MAGs) spanning more than 45 phyla and discovered the first extremophilic members of the Candidate Phyla Radiation (CPR). Five new species of CPR were among the most dominant community members. Novel dominant lineages were found within previously well-characterized functional groups involved in carbon, sulfur, and nitrogen cycling. Moreover, key enzymes of the Wood-Ljungdahl pathway were encoded within at least four bacterial phyla never previously associated with this ancient anaerobic pathway for carbon fixation and dissimilation, including the Actinobacteria. CONCLUSIONS: Our first sequencing effort of hypersaline soda lake sediment metagenomes led to two important advances. First, we showed the existence and obtained the first genomes of haloalkaliphilic members of the CPR and several hundred other novel prokaryote lineages. The soda lake CPR is a functionally diverse group, but the most abundant organisms in this study are likely fermenters with a possible role in primary carbon degradation. Second, we found evidence for the presence of the Wood-Ljungdahl pathway in many more taxonomic groups than those encompassing known homo-acetogens, sulfate-reducers, and methanogens. Since only few environmental metagenomics studies have targeted sediment microbial communities and never to this extent, we expect that our findings are relevant not only for the understanding of haloalkaline environments but can also be used to set targets for future studies on marine and freshwater sediments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0548-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-61467482018-09-24 A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments Vavourakis, Charlotte D. Andrei, Adrian-Stefan Mehrshad, Maliheh Ghai, Rohit Sorokin, Dimitry Y. Muyzer, Gerard Microbiome Research BACKGROUND: Hypersaline soda lakes are characterized by extreme high soluble carbonate alkalinity. Despite the high pH and salt content, highly diverse microbial communities are known to be present in soda lake brines but the microbiome of soda lake sediments received much less attention of microbiologists. Here, we performed metagenomic sequencing on soda lake sediments to give the first extensive overview of the taxonomic diversity found in these complex, extreme environments and to gain novel physiological insights into the most abundant, uncultured prokaryote lineages. RESULTS: We sequenced five metagenomes obtained from four surface sediments of Siberian soda lakes with a pH 10 and a salt content between 70 and 400 g L(−1). The recovered 16S rRNA gene sequences were mostly from Bacteria, even in the salt-saturated lakes. Most OTUs were assigned to uncultured families. We reconstructed 871 metagenome-assembled genomes (MAGs) spanning more than 45 phyla and discovered the first extremophilic members of the Candidate Phyla Radiation (CPR). Five new species of CPR were among the most dominant community members. Novel dominant lineages were found within previously well-characterized functional groups involved in carbon, sulfur, and nitrogen cycling. Moreover, key enzymes of the Wood-Ljungdahl pathway were encoded within at least four bacterial phyla never previously associated with this ancient anaerobic pathway for carbon fixation and dissimilation, including the Actinobacteria. CONCLUSIONS: Our first sequencing effort of hypersaline soda lake sediment metagenomes led to two important advances. First, we showed the existence and obtained the first genomes of haloalkaliphilic members of the CPR and several hundred other novel prokaryote lineages. The soda lake CPR is a functionally diverse group, but the most abundant organisms in this study are likely fermenters with a possible role in primary carbon degradation. Second, we found evidence for the presence of the Wood-Ljungdahl pathway in many more taxonomic groups than those encompassing known homo-acetogens, sulfate-reducers, and methanogens. Since only few environmental metagenomics studies have targeted sediment microbial communities and never to this extent, we expect that our findings are relevant not only for the understanding of haloalkaline environments but can also be used to set targets for future studies on marine and freshwater sediments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0548-7) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-19 /pmc/articles/PMC6146748/ /pubmed/30231921 http://dx.doi.org/10.1186/s40168-018-0548-7 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Vavourakis, Charlotte D.
Andrei, Adrian-Stefan
Mehrshad, Maliheh
Ghai, Rohit
Sorokin, Dimitry Y.
Muyzer, Gerard
A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
title A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
title_full A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
title_fullStr A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
title_full_unstemmed A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
title_short A metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
title_sort metagenomics roadmap to the uncultured genome diversity in hypersaline soda lake sediments
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6146748/
https://www.ncbi.nlm.nih.gov/pubmed/30231921
http://dx.doi.org/10.1186/s40168-018-0548-7
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