Electronic versions

  • Eleanor Jameson
    School of Health and Life Sciences , Teesside University , Middlesbrough , UKThe University of Warwick
  • Jason Stephenson
    The University of Warwick
  • Helen Jones
    School of Health and Life Sciences , Teesside University , Middlesbrough , UKThe University of Warwick
  • Andrew Millard
    Leicester University
  • Anne-Kristin Kaster
    Karlsruhe Institute of Technology
  • Kevin J Purdy
    The University of Warwick
  • Ruth Airs
    Plymouth Marine Laboratory
  • J Colin Murrell
    The University of East Anglia
  • Yin Chen
    The University of Warwick

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.

Keywords

  • Choline/metabolism, Deltaproteobacteria/genetics, Geologic Sediments/microbiology, High-Throughput Nucleotide Sequencing, Metagenome, Metagenomics, Methane/metabolism, Methanosarcinaceae/genetics, Methylamines/metabolism, RNA, Ribosomal, 16S/genetics, Wetlands
Original languageEnglish
Pages (from-to)277-289
Number of pages13
JournalThe ISME Journal
Volume13
Issue number2
Early online date11 Sept 2018
DOIs
Publication statusPublished - 1 Feb 2019
Externally publishedYes
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