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A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments

BACKGROUND: Coastal environments are dynamic and rapidly changing. Living organisms in coastal environments are known to synthesise large quantities of organic osmolytes, which they use to cope with osmotic stresses. The organic osmolyte glycine betaine (GBT) is ubiquitously found in marine biota fr...

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Autores principales: Jones, Helen J., Kröber, Eileen, Stephenson, Jason, Mausz, Michaela A., Jameson, Eleanor, Millard, Andrew, Purdy, Kevin J., Chen, Yin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716910/
https://www.ncbi.nlm.nih.gov/pubmed/31464644
http://dx.doi.org/10.1186/s40168-019-0732-4
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author Jones, Helen J.
Kröber, Eileen
Stephenson, Jason
Mausz, Michaela A.
Jameson, Eleanor
Millard, Andrew
Purdy, Kevin J.
Chen, Yin
author_facet Jones, Helen J.
Kröber, Eileen
Stephenson, Jason
Mausz, Michaela A.
Jameson, Eleanor
Millard, Andrew
Purdy, Kevin J.
Chen, Yin
author_sort Jones, Helen J.
collection PubMed
description BACKGROUND: Coastal environments are dynamic and rapidly changing. Living organisms in coastal environments are known to synthesise large quantities of organic osmolytes, which they use to cope with osmotic stresses. The organic osmolyte glycine betaine (GBT) is ubiquitously found in marine biota from prokaryotic Bacteria and Archaea to coastal plants, marine protozoa, and mammals. In intertidal coastal sediment, GBT represents an important precursor of natural methane emissions and as much as 90% of total methane production in these ecosystems can be originated from methanogenesis from GBT and its intermediate trimethylamine through microbial metabolism. RESULTS: We set out to uncover the microorganisms responsible for methanogenesis from GBT using stable isotope labelling and metagenomics. This led to the recovery of a near-complete genome (2.3 Mbp) of a novel clostridial bacterium involved in anaerobic GBT degradation. Phylogenetic analyses of 16S rRNA gene, functional marker genes, and comparative genomics analyses all support the establishment of a novel family Candidatus ‘Betainaceae’ fam. nov. in Clostridiales and its role in GBT metabolism. CONCLUSIONS: Our comparative genomes and metagenomics analyses suggest that this bacterium is widely distributed in coastal salt marshes, marine sediments, and deep subsurface sediments, suggesting a key role of anaerobic GBT metabolism by this clostridial bacterium in these ecosystems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0732-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-67169102019-09-04 A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments Jones, Helen J. Kröber, Eileen Stephenson, Jason Mausz, Michaela A. Jameson, Eleanor Millard, Andrew Purdy, Kevin J. Chen, Yin Microbiome Research BACKGROUND: Coastal environments are dynamic and rapidly changing. Living organisms in coastal environments are known to synthesise large quantities of organic osmolytes, which they use to cope with osmotic stresses. The organic osmolyte glycine betaine (GBT) is ubiquitously found in marine biota from prokaryotic Bacteria and Archaea to coastal plants, marine protozoa, and mammals. In intertidal coastal sediment, GBT represents an important precursor of natural methane emissions and as much as 90% of total methane production in these ecosystems can be originated from methanogenesis from GBT and its intermediate trimethylamine through microbial metabolism. RESULTS: We set out to uncover the microorganisms responsible for methanogenesis from GBT using stable isotope labelling and metagenomics. This led to the recovery of a near-complete genome (2.3 Mbp) of a novel clostridial bacterium involved in anaerobic GBT degradation. Phylogenetic analyses of 16S rRNA gene, functional marker genes, and comparative genomics analyses all support the establishment of a novel family Candidatus ‘Betainaceae’ fam. nov. in Clostridiales and its role in GBT metabolism. CONCLUSIONS: Our comparative genomes and metagenomics analyses suggest that this bacterium is widely distributed in coastal salt marshes, marine sediments, and deep subsurface sediments, suggesting a key role of anaerobic GBT metabolism by this clostridial bacterium in these ecosystems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0732-4) contains supplementary material, which is available to authorized users. BioMed Central 2019-08-27 /pmc/articles/PMC6716910/ /pubmed/31464644 http://dx.doi.org/10.1186/s40168-019-0732-4 Text en © The Author(s). 2019 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
Jones, Helen J.
Kröber, Eileen
Stephenson, Jason
Mausz, Michaela A.
Jameson, Eleanor
Millard, Andrew
Purdy, Kevin J.
Chen, Yin
A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
title A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
title_full A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
title_fullStr A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
title_full_unstemmed A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
title_short A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
title_sort new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716910/
https://www.ncbi.nlm.nih.gov/pubmed/31464644
http://dx.doi.org/10.1186/s40168-019-0732-4
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