Abstract
Dimethylsulfoniopropionate (DMSP) is a ubiquitous organosulfur compound in marine environments with important functions in both microorganisms and global biogeochemical carbon and sulfur cycling. The SAR11 clade and marine Roseobacter group (MRG) represent two major groups of heterotrophic bacteria in Earth's surface oceans, which can accumulate DMSP to high millimolar intracellular concentrations. However, few studies have investigated how SAR11 and MRG bacteria import DMSP. Here, through comparative genomics analyses, genetic manipulations, and biochemical analyses, we identified an ABC (ATP-binding cassette)-type DMSP-specific transporter, DmpXWV, in Ruegeria pomeroyi DSS-3, a model strain of the MRG. Mutagenesis suggested that DmpXWV is a key transporter responsible for DMSP uptake in strain DSS-3. DmpX, the substrate binding protein of DmpXWV, had high specificity and binding affinity towards DMSP. Furthermore, the DmpX DMSP-binding mechanism was elucidated from structural analysis. DmpX proteins are prevalent in the numerous cosmopolitan marine bacteria outside the SAR11 clade and the MRG, and dmpX transcription was consistently high across Earth's entire global ocean. Therefore, DmpXWV likely enables pelagic marine bacteria to efficiently import DMSP from seawater. This study offers a new understanding of DMSP transport into marine bacteria and provides novel insights into the environmental adaption of marine bacteria.
Original language | English |
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Pages (from-to) | 579-587 |
Number of pages | 9 |
Journal | The ISME Journal |
Volume | 17 |
Issue number | 4 |
Early online date | 27 Jan 2023 |
DOIs | |
Publication status | Published - Apr 2023 |
Bibliographical note
Funding:This work was supported by the National Key Research and Development Program of China (2022YFC2807500, 2021YFA0909600), the National Science Foundation of China (grants 92251303, 91851205, 42276102, 42076229, 31961133016), the Fundamental Research Funds for the Central Universities (202172002, 202041011), Major Scientific and Technological Innovation Project (MSTIP) of Shandong Province (2019JZZY010817), the Program of Shandong for Taishan Scholars (tspd20181203), and Natural Environment Research Council, UK, Standard grants (NE/X000990, NE/V000756, and NE/S001352) and the Leverhulme Trust research grant (RPG-2020-413).
Copyright:
© 2023. The Author(s).
Keywords
- ATP-Binding Cassette Transporters/genetics
- Seawater/microbiology
- Oceans and Seas
- Sulfonium Compounds/metabolism