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Deltaproteobacteria (Pelobacter) and Methanococcoides are responsible for choline-dependent methanogenesis in a coastal saltmarsh sediment.

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posted on 08.07.2019, 14:38 by E Jameson, J Stephenson, H Jones, A Millard, A-K Kaster, KJ Purdy, R Airs, JC Murrell, Y Chen
Coastal saltmarsh sediments represent an important source of natural methane emissions, much of which originates from quaternary and methylated amines, such as choline and trimethylamine. In this study, we combine DNA stable isotope probing with high throughput sequencing of 16S rRNA genes and 13C2-choline enriched metagenomes, followed by metagenome data assembly, to identify the key microbes responsible for methanogenesis from choline. Microcosm incubation with 13C2-choline leads to the formation of trimethylamine and subsequent methane production, suggesting that choline-dependent methanogenesis is a two-step process involving trimethylamine as the key intermediate. Amplicon sequencing analysis identifies Deltaproteobacteria of the genera Pelobacter as the major choline utilizers. Methanogenic Archaea of the genera Methanococcoides become enriched in choline-amended microcosms, indicating their role in methane formation from trimethylamine. The binning of metagenomic DNA results in the identification of bins classified as Pelobacter and Methanococcoides. Analyses of these bins reveal that Pelobacter have the genetic potential to degrade choline to trimethylamine using the choline-trimethylamine lyase pathway, whereas Methanococcoides are capable of methanogenesis using the pyrrolysine-containing trimethylamine methyltransferase pathway. Together, our data provide a new insight on the diversity of choline utilizing organisms in coastal sediments and support a syntrophic relationship between Bacteria and Archaea as the dominant route for methanogenesis from choline in this environment.

Funding

This work was supported by the Natural Environment Research Council (NERC), UK, through research grants (NE/I027061/1 and NE/I025077/1) and a Ph.D. studentship to H.J. and a Warwick Integrative Synthetic Biology (WISB) early career fellowship, funded jointly by BBSRC and EPSRC to E.J.

History

Citation

The ISME Journal, 2019, 13, pp. 277–289

Author affiliation

/Organisation/COLLEGE OF LIFE SCIENCES/School of Medicine/Department of Infection, Immunity and Inflammation

Version

VoR (Version of Record)

Published in

The ISME Journal

Publisher

Springer Nature for International Society for Microbial Ecology

eissn

1751-7370

Acceptance date

26/07/2018

Copyright date

2018

Available date

08/07/2019

Publisher version

https://www.nature.com/articles/s41396-018-0269-8

Notes

The online version of this article (https://doi.org/10.1038/s41396-018-0269-8) contains supplementary material, which is available to authorized users.

Language

en

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