Dimethylsulfoniopropionate Turnover Is Linked to the Composition and Dynamics of the Bacterioplankton Assemblage during a Microcosm Phytoplankton Bloom

Abstract

Processing of the phytoplankton-derived organic sulfur compound dimethylsulfoniopropionate (DMSP) by bacteria was studied in seawater microcosms in the coastal Gulf of Mexico (Alabama). Modest phytoplankton blooms (peak chlorophyll a [Chl a] concentrations of ϳ2.5 g liter ؊1 ) were induced in nutrient-enriched microcosms, while phytoplankton biomass remained low in unamended controls (Chl a concentrations of ϳ0.34 g liter ؊1 ). Particulate DMSP concentrations reached 96 nM in the enriched microcosms but remained approximately 14 nM in the controls. Bacterial biomass production increased in parallel with the increase in particulate DMSP, and nutrient limitation bioassays in the initial water showed that enrichment with DMSP or glucose caused a similar stimulation of bacterial growth. Concomitantly, increased bacterial consumption rate constants of dissolved DMSP (up to 20 day ؊1 ) and dimethylsulfide (DMS) (up to 6.5 day ؊1 ) were observed. Nevertheless, higher DMSP S assimilation efficiencies and higher contribution of DMSP to bacterial S demand were found in the controls compared to the enriched microcosms. This indicated that marine bacterioplankton may rely more on DMSP as a source of S under oligotrophic conditions than under the senescence phase of phytoplankton blooms. Phylogenetic analysis of the bacterial assemblages in all microcosms showed that the DMSP-rich algal bloom favored the occurrence of various Roseobacter members, flavobacteria (Bacteroidetes phylum), and oligotrophic marine Gammaproteobacteria. Our observations suggest that the composition of the bacterial assemblage and the relative contribution of DMSP to the overall dissolved organic sulfur/organic matter pool control how efficiently bacteria assimilate DMSP S and thereby potentially divert it from DMS production.During blooms of phytoplankton, and particularly during their senescence, the activity of bacterioplankton is stimulated by the release of dissolved organic matter (DOM) and nutrients. Since bacterioplankton groups differ in their growth requirements, such release can stimulate the growth of specific components of the bacterioplankton assemblage. Given that bacterial taxa differ in their potential for hydrolytic ectoenzyme activities and their capacity to assimilate and process various substrates (10, 22), shifts in the composition of bacterioplankton assemblages under phytoplankton blooms or oligotrophic conditions are likely to have consequences for the turnover of organic matter and biogeochemically active elements such as N and S.A component of the DOM pool that has attracted much attention for the last two decades is the algal osmolyte dimethylsulfoniopropionate (DMSP). This sulfur-containing compound is released into the water column, where it plays important roles in C and S cycling, through algal lysis or zooplankton predation. A volatile degradation product of DMSP (dimethylsulfide [DMS]) escapes to the atmosphere, where it influences climate through cloud formation (1). Bacterial utilization of DMSP is also important an...

Revising upper-ocean sulfur dynamics near Bermuda: new lessons from 3 years of concentration and rate measurements

“…[39] The values observed at the oligotrophic BATS site were significantly lower than the turnover rates observed in coastal, high iron rich waters (22.1 day À1 ) [39] and in an enriched mesocosm experiment (,20 day À1 ). [40] Although slightly lower values were observed below the mixed layer in the summer, k DMSP did not have a defined seasonal cycle, in contrast to DMSPp and, to a lesser extent, DMSPd (Figs 4, 5). In addition, no relationship was observed between k DMSP and [DMSPd], [DMSPp] or bacterial production rates, nor was there a correlation between dDMSPd/dt and bacterial production (Fig.…”

Single-taxon field measurements of bacterial gene regulation controlling DMSP fate

“…When DMSP accounts for a small percentage of phytoplankton C (October 4-6) and alternate organic S compounds are present, dddP is upregulated to bias metabolism towards the cleavage pathway, satisfying the cells' requirements with non-DMSP organic sulfur and avoiding ROS stress generated during demethylation. Pinhassi et al, 2005), bacteria preferentially use the demethylation pathway to meet their biosynthetic requirements; but when alternate organic sulfur compounds are more available, the cleavage pathway is favored because DMSP-sulfur is no longer necessary for biosynthesis (Pinhassi et al, 2005;Merzouk et al, 2006Merzouk et al, , 2008Lizotte et al, 2009;Rinta-Kanto et al, 2011). The availability of DMSP to marine bacteria is influenced by the taxonomy of the dominant phytoplankton because the percent contribution of DMSP to carbon in phytoplankton (%DMSP-C; varies among taxonomic groups.…”

“…Wide variation in the percent of dissolved DMSP converted to DMS in ocean surface waters (3% to 30%; has most frequently been attributed to the energetic benefit to bacteria of acquiring pre-reduced sulfur rather than expending three ATP equivalents to reduce seawater sulfate Pinhassi et al, 2005;Moran et al, 2012). This 'bacterial sulfur demand' hypothesis proposes that demethylation is favored by marine bacteria when reduced sulfur is limiting because the sulfur from DMSP can be assimilated into biomass through the demethylation pathway but not the cleavage pathway (Todd et al, 2009).…”

Determining indicator taxa across spatial and seasonal gradients in the Columbia River coastal margin

“…This sequence was identical to clones from the Delaware Bay (Shaw et al, 2008) and was nearly identical (99%) to Roseobacter sp. clones from the Gulf of Mexico (Pinhassi et al, 2005), demonstrating that this taxon is prevalent in coastal oceaninfluenced environments as seen in later months in the Columbia River estuary. In the plume, the community composition was less correlated with river specific variables like river flow and residence time, and more with seasonal variables like temperature, leading to a distinct bacterioplankton community in the summer months.…”