TY - JOUR

T1 - A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments

AU - Jones, Helen J

AU - Kröber, Eileen

AU - Stephenson, Jason

AU - Mausz, Michaela A

AU - Jameson, Eleanor

AU - Millard, Andrew

AU - Purdy, Kevin J

AU - Chen, Yin

PY - 2019/8/27

Y1 - 2019/8/27

N2 - 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.

AB - 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.

KW - Bacteria/classification

KW - Betaine/metabolism

KW - Geologic Sediments/microbiology

KW - Metagenomics

KW - Methane/metabolism

KW - Osmosis

KW - Phylogeny

KW - RNA, Ribosomal, 16S/genetics

KW - Seawater/microbiology

KW - United Kingdom

KW - Wetlands

U2 - 10.1186/s40168-019-0732-4

DO - 10.1186/s40168-019-0732-4

M3 - Article

C2 - 31464644

VL - 7

JO - Microbiome

JF - Microbiome

SN - 2049-2618

IS - 1

M1 - 120

ER -