A new dimethylsulfoniopropionate lyase of the cupin superfamily in marine bacteria

Abstract

Dimethylsulfoniopropionate (DMSP) is a marine organosulfur compound with important roles in stress protection, marine biogeochemical cycling, chemical signalling and atmospheric chemistry. Diverse marine microorganisms catabolize DMSP via DMSP lyases to generate the climate-cooling gas and info-chemical dimethyl sulphide. Abundant marine heterotrophs of the Roseobacter group (MRG) are well known for their ability to catabolize DMSP via diverse DMSP lyases. Here, a new DMSP lyase DddU within the MRG strain Amylibacter cionae H-12 and other related bacteria was identified. DddU is a cupin superfamily DMSP lyase like DddL, DddQ, DddW, DddK and DddY, but shares <15% amino acid sequence identity with these enzymes. Moreover, DddU proteins forms a distinct clade from these other cupin-containing DMSP lyases. Structural prediction and mutational analyses suggested that a conserved tyrosine residue is the key catalytic amino acid residue in DddU. Bioinformatic analysis indicated that the dddU gene, mainly from Alphaproteobacteria, is widely distributed in the Atlantic, Pacific, Indian and polar oceans. For reference, dddU is less abundant than dddP, dddQ and dddK, but much more frequent than dddW, dddY and dddL in marine environments. This study broadens our knowledge on the diversity of DMSP lyases, and enhances our understanding of marine DMSP biotransformation.

On the Substrate Scope of Dimethylsulfonium Propionate Lyases toward Dimethylsulfoxonium Propionate Derivatives

“…DMSP is a long known marine metabolite and several DMSP lyases have been described in the literature for its cleavage into the climatically relevant gas dimethyl sulfide. [27][28][29][30][31][32][33][34] Recently, the oxidized derivative DMSOP was discovered in the marine environment that may play a similarly important role in the marine sulfur metabolism as DMSP. As we [40] and others [41] have shown, DMSOP can also be cleaved by DMSP lyases.…”

“…[24] The cleavage of DMS from DMSP by bacteria is either catalyzed by the type III acyl-CoA transferase DddD with hydrolytic DMS release from a covalently enzyme bound intermediate with formation of 3-hydroxypropionate (1, Scheme 1A), [25,26] or by one of the distinct DMSP lyases (DddL, DddP, DddQ, DddY, DddW, DddK and DddU) that have been reported to date. [27][28][29][30][31][32][33] In addition, the DMSP lyase Alma1 is known from the coccolithophore Emiliania huxleyi. [34] All these DMSP lyases cause the elimination of DMS with formation of acrylate (2).…”

Dimethylsulfoniopropionate (DMSP) Increases Longevity and Mitochondrial Function in Caenorhabditis elegans: Implications for the Role of the Global Sulfur Cycle in Terrestrial Ecosystems

“…2−4 In addition, marine bacteria metabolize DMSP, resulting in the release of DMS and other compounds into the surrounding seawater. 5 Eventually, through a process known as "sea-to-air flux," DMS is emitted into the atmosphere, primarily at the ocean's surface through diffusion. 6 Once in the atmosphere, DMS undergoes chemical reactions driven primarily by sunlight and atmospheric oxidants.…”

“…Dimethylsulfoniopropionate (DMSP), an algal compound that serves as a precursor for the climate-relevant volatile dimethyl sulfide (DMS), is involved in various roles in the ocean. It is produced naturally by marine phytoplankton, macroalgae, and some bacteria. − In addition, marine bacteria metabolize DMSP, resulting in the release of DMS and other compounds into the surrounding seawater . Eventually, through a process known as “sea-to-air flux,” DMS is emitted into the atmosphere, primarily at the ocean’s surface through diffusion .…”

Developing a Base Editing System for Marine Roseobacter Clade Bacteria

“…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.…”