Microdiversity and temporal dynamics of marine bacterial dimethylsulfoniopropionate genes

Abstract

Summary Dimethylsulfoniopropionate (DMSP) is an abundant organic sulfur metabolite produced by many phytoplankton species and degraded by bacteria via two distinct pathways with climate‐relevant implications. We assessed the diversity and abundance of bacteria possessing these pathways in the context of phytoplankton community composition over a 3‐week time period spanning September–October, 2014 in Monterey Bay, CA. The dmdA gene from the DMSP demethylation pathway dominated the DMSP gene pool and was harboured mostly by members of the alphaproteobacterial SAR11 clade and secondarily by the Roseobacter group, particularly during the second half of the study. Novel members of the DMSP‐degrading community emerged from dmdA sequences recovered from metagenome assemblies and single‐cell sequencing, including largely uncharacterized gammaproteobacteria and alphaproteobacteria taxa. In the DMSP cleavage pathway, the SAR11 gene dddK was the most abundant early in the study, but was supplanted by dddP over time. SAR11 members, especially those harbouring genes for both DMSP degradation pathways, had a strong positive relationship with the abundance of dinoflagellates, and DMSP‐degrading gammaproteobacteria co‐occurred with haptophytes. This in situ study of the drivers of DMSP fate in a coastal ecosystem demonstrates for the first time correlations between specific groups of bacterial DMSP degraders and phytoplankton taxa.

Seasonal dynamics of marine snow‐associated and free‐living demethylating bacterial communities in the coastal northern Adriatic Sea

“…The patchy distribution of subclade D/3 in the AW might also indicate that the representative bacterial group (SAR11 clade) consists of many ecotypes with fine‐tuned adaptations to physical and chemical gradients (Carlson et al ., ). The SAR11 clade consists of members highly active in DMSP degradation correlating with haptophyte abundance (including coccolithophores) (Nowinski et al ., ). In this study, subclade D/3 was present in June, when coccolithophores were abundant and DMSPt + DMS concentrations high.…”

“…It is released from phytoplankton into the ambient water and is subsequently degraded by bacteria either via the DMSP cleavage or demethylation pathway (Kiene et al ., ; Moran et al ., ). Diverse taxa of marine bacteria can mediate one or the other, or both processes (Simó, ; Reisch et al ., ; Moran et al ., ; Varaljay et al ., ; Nowinski et al ., ), thereby controlling the fate of dissolved DMSP in the ocean. Genes of the demethylation pathway have been found in 2‐ to about 5‐fold higher abundance than genes of the cleavage pathway in metagenomes obtained from the Global Ocean Survey (Moran et al ., ), at Station ALOHA (Varaljay et al ., ) and Monterey Bay (Nowinski et al ., ).…”

“…Diverse taxa of marine bacteria can mediate one or the other, or both processes (Simó, ; Reisch et al ., ; Moran et al ., ; Varaljay et al ., ; Nowinski et al ., ), thereby controlling the fate of dissolved DMSP in the ocean. Genes of the demethylation pathway have been found in 2‐ to about 5‐fold higher abundance than genes of the cleavage pathway in metagenomes obtained from the Global Ocean Survey (Moran et al ., ), at Station ALOHA (Varaljay et al ., ) and Monterey Bay (Nowinski et al ., ). Approximately 90% of dissolved DMSP in the ocean is demethylated (Kiene et al ., ; Kiene and Linn, ), implicating that the sulfur moieties are not lost to the atmosphere via dimethylsulfide (DMS), but rather enter the marine food web (Moran et al ., ).…”

“…Total DMSP concentrations in the ocean depend largely on the abundance and intracellular DMSP concentrations of the main DMSP‐producing phytoplankton taxa (Keller et al ., ) but also on environmental factors such as salinity, grazing pressure and nutrient concentrations (Stefels et al ., ). Responses of demethylating bacteria to phytoplankton blooms (Howard et al ., ), specific phytoplankton taxa (Howard et al ., ; Varaljay et al ., ) and to DMSP concentrations (Frade et al ., ; Nowinski et al ., ) indicate that demethylating bacteria can occupy a wide range of niches. Specific subclades of the dmd A gene, responsible for the demethylation of DMSP, have been found in different size fractions of coastal waters, suggesting that bacteria with contrasting lifestyles, such as free‐living versus particle‐attached, could potentially demethylate DMSP (Varaljay et al ., ).…”

Marine snow as a habitat for microbial mercury methylators in the Baltic Sea

“…However, a recent 51 work has unravelled a higher phylogenetic diversity of microbes carrying the hgcAB genes than 52 previously expected (McDaniel et al, 2020) and this calls for novel analyses of microbial Hg-53 methylation in aquatic environments. 54 55 Recent advances in metagenomics have yielded new insights into the microbial taxonomic and 56 functional diversity in various aquatic ecosystems (e.g., Mehrshad et al, 2016;Haro-Moreno et al, 57 2018; Nowinski et al, 2019). The approach has for example been applied to broadly assess the 58 presence and diversity of genes central to biological Hg cycling in marine systems (Podar et al,59 2015; Gionfriddo et al, 2016;Bowman et al, 2019;Villar et al, 2020).…”