Frontiers Science Center for Deep Ocean Multispheres and Earth System & College of Marine Life Sciences, Ocean University of China, Qingdao, China.
State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China.
ISME J. 2023 Apr;17(4):579-587. doi: 10.1038/s41396-023-01375-3. Epub 2023 Jan 27.
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.
二甲基巯基丙酸酯 (DMSP) 是海洋环境中普遍存在的有机硫化合物,在微生物和全球生物地球化学碳和硫循环中具有重要功能。SAR11 丛和海洋玫瑰杆菌群 (MRG) 代表了地球表面海洋中两种主要的异养细菌群体,它们可以将 DMSP 积累到高毫摩尔细胞内浓度。然而,很少有研究探讨 SAR11 和 MRG 细菌如何摄取 DMSP。在这里,通过比较基因组学分析、遗传操作和生化分析,我们在 Ruegeria pomeroyi DSS-3 中鉴定出一种 ABC(ATP 结合盒)型 DMSP 特异性转运蛋白 DmpXWV,DSS-3 是 MRG 的模式菌株。突变分析表明,DmpXWV 是负责 DSS-3 菌株摄取 DMSP 的关键转运蛋白。DmpXWV 的底物结合蛋白 DmpX 对 DMSP 具有高特异性和结合亲和力。此外,还通过结构分析阐明了 DmpX 结合 DMSP 的机制。DmpX 蛋白在 SAR11 丛和 MRG 之外的众多世界性海洋细菌中普遍存在,并且 dmpX 转录在整个地球海洋中始终保持较高水平。因此,DmpXWV 可能使浮游海洋细菌能够从海水中有效地摄取 DMSP。本研究为 DMSP 向海洋细菌的转运提供了新的认识,并为海洋细菌的环境适应提供了新的见解。