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


Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
27 08 2019
Historique:
received: 08 07 2019
accepted: 13 08 2019
entrez: 30 8 2019
pubmed: 30 8 2019
medline: 27 5 2020
Statut: epublish

Résumé

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. 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. 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.

Sections du résumé

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.

Identifiants

pubmed: 31464644
doi: 10.1186/s40168-019-0732-4
pii: 10.1186/s40168-019-0732-4
pmc: PMC6716910
doi:

Substances chimiques

RNA, Ribosomal, 16S 0
Betaine 3SCV180C9W
Methane OP0UW79H66

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

120

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Auteurs

Helen J Jones (HJ)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.

Eileen Kröber (E)

Microbial Biogeochemistry, RA Landscape Functioning, ZALF Leibniz Centre for Agricultural Landscape Research, 15374, Müncheberg, Germany. eileen.kroeber@zalf.de.

Jason Stephenson (J)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.

Michaela A Mausz (MA)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.

Eleanor Jameson (E)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.

Andrew Millard (A)

Department of Infection, Immunity and Inflammation, University of Leicester, Leicester, LE1 7RH, UK.

Kevin J Purdy (KJ)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK.

Yin Chen (Y)

School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK. Y.Chen.25@warwick.ac.uk.

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Classifications MeSH