Ubiquitous occurrence of a dimethylsulfoniopropionate ABC transporter in abundant marine bacteria

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.

Developing a Base Editing System for Marine Roseobacter Clade Bacteria

“…Besides the utilization of aromatic carbon, roseobacters are also essential for the marine sulfur cycle and important in microbial ecology in the ocean. 11,34 With an efficient and precise genome editing tool, bacteria in the Roseobacter clade can be an experimental chassis with indispensable biogeochemical roles for the evaluation of environmental and ecological impacts of global climate change and emerging pollutants (e.g., plastics) in the ocean.…”

“…Since the genus Roseobacter was coined in 1991, the evolution and ecology of the Roseobacter clade have been investigated mainly with biochemistry and omics approaches. ,, Methods for genetic manipulation of the Roseobacter clade bacteria have also been established to construct mutants of different roseobacters. , These methods include DNA delivery, e.g., conjugation and electroporation, and the knock-in genome editing based on homology-directed repair (HDR) and selective markers (e.g., antibiotic resistance genes) . Despite these advances, current methods seem to be stopped at the conventional approaches, which can hardly meet the increasing requirement of precise genetic manipulation for scientific discovery and technology development in the Roseobacter clade.…”

Bacterial catabolism of membrane phospholipids links marine biogeochemical cycles

“…Marine DOM comprises complex biopolymers that require specific molecular mechanisms to perform extracellular hydrolysis and subsequent high affinity transport (38,39,(42)(43)(44). Metabolites are then shared in mutualistic or competing relationships (45,46). Despite the myriad of metabolites comprising the DOM pool (47) and the importance of metabolic "sharing" between marine microbes, the molecular mechanisms underpinning the breakdown of these metabolites remain poorly characterized although their mineralization is key to these interactions.…”

“…If we assume that etoX expression is a proxy for phosphatase-dependent PE hydrolysis, then the ubiquitous expression of etoX across all oceanic sites and depths, from mesopelagic through to surface waters with maximal expression at the deep chlorophyll maximum ( Fig. 6B ), suggests that PE turnover is constantly occurring throughout the global ocean at a scale comparable to other well-known nutrients ( 27 , 39 , 43 , 46 , 54 ). While homologs of betT are also abundant and highly expressed, with maximal expression in mesopelagic waters, this BCCT-type transporter is usually nonspecific for various osmolytes, and caution regarding the importance of PC and choline in open ocean waters should be taken ( 31 , 52 ).…”

Ultrahigh-affinity transport proteins from ubiquitous marine bacteria reveal mechanisms and global patterns of nutrient uptake

“…Furthermore, due to the genetic intractability of SAR11 bacteria, the observed transport activity cannot be linked to specific ABC transporter genes, limiting integration of the resulting physiological data with existing multi-omics datasets to uncover the broader geochemical and ecological significance of transport activity. An alternative approach to elucidate the functions of ABC transporters is through biochemical characterization of the corresponding SBPs 21 , which relies on the fact that the specificity and affinity of nutrient uptake by ABC transporters is mainly determined by the binding specificity and affinity of the corresponding SBPs 22 , and has been demonstrated to be a valuable method for discovery of new metabolic pathways, particularly by the Enzyme Function Initiative project 23,24 .…”