Evolutionary history of dimethylsulfoniopropionate (DMSP) demethylation enzyme DmdA in marine bacteria

Abstract

Dimethylsulfoniopropionate (DMSP), an osmolyte produced by oceanic phytoplankton and bacteria, is primarily degraded by bacteria belonging to the Roseobacter lineage and other marine Alphaproteobacteria via DMSP-dependent demethylase A protein (DmdA). To date, the evolutionary history of DmdA gene family is unclear. Some studies indicate a common ancestry between DmdA and GcvT gene families and a co-evolution between Roseobacter and the DMSP-producing-phytoplankton around 250 million years ago (Mya). In this work, we analyzed the evolution of DmdA under three possible evolutionary scenarios: (1) a recent common ancestor of DmdA and GcvT, (2) a coevolution between Roseobacter and the DMSP-producing-phytoplankton, and (3) an enzymatic adaptation for utilizing DMSP in marine bacteria prior to Roseobacter origin. Our analyses indicate that DmdA is a new gene family originated from GcvT genes by duplication and functional divergence driven by positive selection before a coevolution between Roseobacter and phytoplankton. Our data suggest that Roseobacter acquired dmdA by horizontal gene transfer prior to an environment with higher DMSP. Here, we propose that the ancestor that carried the DMSP demethylation pathway genes evolved in the Archean, and was exposed to a higher concentration of DMSP in a sulfur-rich atmosphere and anoxic ocean, compared to recent Roseobacter eco-orthologs (orthologs performing the same function under different conditions), which should be adapted to lower concentrations of DMSP.

You Exude What You Eat: How Carbon-, Nitrogen-, and Sulfur-Rich Organic Substrates Shape Microbial Community Composition and the Dissolved Organic Matter Pool

“…In contrast, Rhodobacterales was positively associated with S-containing formulas and relative labile protein-like C1 component and negatively associated with MLB R . This fits well with previous findings demonstrating links between members of the Rhodobacteraceae family and sulfur metabolites (47,72), but it also suggests that Rhodobacterales might be less competitive when the substrates are relatively more recalcitrant. Glucose assimilation results in biomass and energy production but also in the synthesis of other metabolic intermediates (e.g., amino acids and fatty acids) needed for bacterial growth (73,74).…”

“…The success of Alteromonadales in utilizing glucose could be due to the phosphoenolpyruvate carboxylase strategy in Gammaproteobacteria instead of the pyruvate carboxylase in Alphaproteobacteria (44), giving them a competitive advantage. In contrast, the degradation of the more complex GBT and DMSP substrates requires specific transporters and enzymes (e.g., betaine-homocysteine methyltransferase and DMSP-dependent demethylase A protein), resulting in the dominance of Alphaproteobacteria (mostly Rhodobacteraceae) with a smaller contribution of the Gammaproteobacterial members (45)(46)(47). Previous studies have also shown that Alphaproteobacteria can account for up to 30% of total bacteria assimilating DMSP in natural environments (48).…”

Development of bacterial resistance induced by low concentration of two-dimensional black phosphorus via mutagenesis

“… 7 Nearly all known DMSP-catabolizing bacteria belong to the phylum Proteobacteria with dmdA , and dmdA gene could be transferred horizontally in marine Gammaproteobacteria. 34 However, few studies have reported that bacteria have mutations in dmdA genes. Thus, the effect of dmdA gene mutation on E. coli needs to be further explored in the future.…”

Missing microbial eukaryotes and misleading meta-omic conclusions

“…Protein prediction was performed with Prodigal 39,63 . The taxonomic identity of predicted proteins was obtained using EUKulele v2.0.3 19 , first using a combined database containing the MMETSP 27,29,36 , MarRef 64 , and additional Phaeocystis references, including the genome resources for Phaeocystis antarctica and Phaeocystis globosa 65,66 available from the IMG/M (Integrated Microbial Genomes & Microbiomes) database (Phaant1 and Phaglo1, respectively), Phaeocystis cordata, Phaeocystis jahnii, and Phaeocystis globosa transcriptome resources [67][68][69] , and a Phaeocystis pouchetii transcriptome (Mars Brisbin et al in prep). The contigs associated with the proteins identified to the genus Phaeocystis were quantified against the raw reads using the CoverM software in contig mode (v0.6.2; https://github.com/wwood/CoverM; coverm contig --min-covered-fraction 0).…”