Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria

Li, Chun-Yang, Mausz, Michaela A., Murphy, Andrew, Zhang, Nan, Chen, Xiu-Lan, Wang, Shu-Yan, Gao, Chao, Aguilo-Ferretjans, María M., Silvano, Eleonora, Lidbury, Ian D. E. A., Fu, Hui-Hui, Todd, Jonathan D., Chen, Yin and Zhang, Yu-Zhong (2023) Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria. ISME Journal, 17 (4). pp. 579-587. ISSN 1751-7362

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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.

Item Type: Article
Additional Information: Data Availability Statement: The structure of RnDmpX/DMSP complex has been deposited in the PDB under the accession codes 7YLE. Funding Information: 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).
Uncontrolled Keywords: microbiology,ecology, evolution, behavior and systematics,sdg 14 - life below water ,/dk/atira/pure/subjectarea/asjc/2400/2404
Faculty \ School: Faculty of Science > School of Biological Sciences
UEA Research Groups: Faculty of Science > Research Groups > Molecular Microbiology
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 14 Jan 2025 00:59
Last Modified: 20 Jan 2025 01:07
URI: https://ueaeprints.uea.ac.uk/id/eprint/98193
DOI: 10.1038/s41396-023-01375-3

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