Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater

Liu, Jingli, Xue, Chun-Xu, Wang, Jinyan, Crombie, Andrew T., Carrión, Ornella, Johnston, Andrew W. B., Murrell, J. Colin, Liu, Ji, Zheng, Yanfen, Zhang, Xiao-Hua and Todd, Jonathan D. (2022) Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater. Microbiome, 10. ISSN 2049-2618

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Abstract

Background: Ubiquitous and diverse marine microorganisms utilise the abundant organosulfur molecule dimethylsulfoniopropionate (DMSP), the main precursor of the climate-active gas dimethylsulfide (DMS), as a source of carbon, sulfur and/or signalling molecules. However, it is currently difficult to discern which microbes actively catabolise DMSP in the environment, why they do so and the pathways used. Results: Here, a novel DNA-stable isotope probing (SIP) approach, where only the propionate and not the DMS moiety of DMSP was 13C-labelled, was strategically applied to identify key microorganisms actively using DMSP and also likely DMS as a carbon source, and their catabolic enzymes, in North Sea water. Metagenomic analysis of natural seawater suggested that Rhodobacterales (Roseobacter group) and SAR11 bacteria were the major microorganisms degrading DMSP via demethylation and, to a lesser extent, DddP-driven DMSP lysis pathways. However, neither Rhodobacterales and SAR11 bacteria nor their DMSP catabolic genes were prominently labelled in DNA-SIP experiments, suggesting they use DMSP as a sulfur source and/or in signalling pathways, and not primarily for carbon requirements. Instead, DNA-SIP identified gammaproteobacterial Oceanospirillales, e.g. Amphritea, and their DMSP lyase DddD as the dominant microorganisms/enzymes using DMSP as a carbon source. Supporting this, most gammaproteobacterial (with DddD) but few alphaproteobacterial seawater isolates grew on DMSP as sole carbon source and produced DMS. Furthermore, our DNA-SIP strategy also identified Methylophaga and other Piscirickettsiaceae as key bacteria likely using the DMS, generated from DMSP lysis, as a carbon source. Conclusions: This is the first study to use DNA-SIP with 13C-labelled DMSP and, in a novel way, it identifies the dominant microbes utilising DMSP and DMS as carbon sources. It highlights that whilst metagenomic analyses of marine environments can predict microorganisms/genes that degrade DMSP and DMS based on their abundance, it cannot disentangle those using these important organosulfur compounds for their carbon requirements. Note, the most abundant DMSP degraders, e.g. Rhodobacterales with DmdA, are not always the key microorganisms using DMSP for carbon and releasing DMS, which in this coastal system were Oceanospirillales containing DddD. [MediaObject not available: see fulltext.].

Item Type: Article
Additional Information: Availability of data and materials 16S rRNA gene amplicon sequencing and metagenomic data generated in this study were deposited to the sequence read archives (SRA) under Bioproject PRJNA685000. The accession numbers for genomes from bacterial strains isolated in this work and MAGs reconstructed from seawater metagenomes are listed in Table 1 and Table S5, respectively. Funding: The work in X-HZ’s lab was funded by the National Natural Science Foundation of China (91751202 and 41730530), the National Key Research and Development Program of China (2016YFA0601303 and 2018YFE0124100), and the Fundamental Research Funds for the Central Universities (202172002). Work in JDT’s lab was funded by the Natural Environment Research Council (NE/P012671, NE/S001352) and the Leverhulme trust (RPG-2020-413) grants.
Uncontrolled Keywords: dimethylsulfoniopropionate (dmsp),dimethylsulfide (dms),dna-stable isotope probing (sip),oceanospirillales,dddd dmsp lyase,seawater,biogeochemical sulfur cycling,dimethylsulfide (dms),biogeochemical sulfur cycling,dna-stable isotope probing (dna-sip),seawater,environmental science(all),immunology and microbiology(all),microbiology (medical),microbiology,sdg 14 - life below water,sdg 13 - climate action,4* ,/dk/atira/pure/subjectarea/asjc/2300
Faculty \ School: Faculty of Science > School of Environmental Sciences
Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 29 Jul 2022 14:30
Last Modified: 12 Aug 2022 04:51
URI: https://ueaeprints.uea.ac.uk/id/eprint/86982
DOI: 10.1186/s40168-022-01304-0

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