The Microbiological Drivers of Temporally Dynamic Dimethylsulfoniopropionate Cycling Processes in Australian Coastal Shelf Waters

Abstract

The organic sulfur compounds dimethylsulfoniopropionate (DMSP) and dimethyl sulfoxide (DMSO) play major roles in the marine microbial food web and have substantial climatic importance as sources and sinks of dimethyl sulfide (DMS). Seasonal shifts in the abundance and diversity of the phytoplankton and bacteria that cycle DMSP are likely to impact marine DMS (O) (P) concentrations, but the dynamic nature of these microbial interactions is still poorly resolved. Here, we examined the relationships between microbial community dynamics with DMS (O) (P) concentrations during a 2-year oceanographic time series conducted on the east Australian coast. Heterogenous temporal patterns were apparent in chlorophyll a (chl a) and DMSP concentrations, but the relationship between these parameters varied over time, suggesting the phytoplankton and bacterial community composition were affecting the net DMSP concentrations through differential DMSP production and degradation. Significant increases in DMSP were regularly measured in spring blooms dominated by predicted high DMSP-producing lineages of phytoplankton (Heterocapsa, Prorocentrum, Alexandrium, and Micromonas), while spring blooms that were dominated by predicted low DMSP-producing phytoplankton (Thalassiosira) demonstrated negligible increases in DMSP concentrations. During elevated DMSP concentrations, a significant increase in the relative abundance of the key copiotrophic bacterial lineage Rhodobacterales was accompanied by a three-fold increase in the gene, encoding the first step of DMSP demethylation (dmdA). Significant temporal shifts in DMS concentrations were measured and were significantly correlated with both fractions (0.2–2 μm and >2 μm) of microbial DMSP lyase activity. Seasonal increases of the bacterial DMSP biosynthesis gene (dsyB) and the bacterial DMS oxidation gene (tmm) occurred during the spring-summer and coincided with peaks in DMSP and DMSO concentration, respectively. These findings, along with significant positive relationships between dsyB gene abundance and DMSP, and tmm gene abundance with DMSO, reinforce the significant role planktonic bacteria play in producing DMSP and DMSO in ocean surface waters. Our results highlight the highly dynamic nature and myriad of microbial interactions that govern sulfur cycling in coastal shelf waters and further underpin the importance of microbial ecology in mediating important marine biogeochemical processes.

Phytoplankton Sources and Sinks of Dimethylsulphoniopropionate (DMSP) in Temperate Coastal Waters of Australia

“…The total DMSP and DMS concentrations measured in this study closely match the annual averages of 25.7 ± 5.31 (DMSPt) and 2.7 ± 0.30 nM (DMS) for Port Hacking measured over a 2-year study and are consistent with, albeit slightly higher than, April DMS/P concentrations for Port Hacking [58]. The relatively high concentration of DMSP measured in the seawater during this study can be attributed to the generally high intracellular concentrations in the DMSP-producing species within the community, including dinoflagellates [59], Phaeocystis sp.…”

The Effect of Zooplankton on the Distributions of Dimethyl Sulfide and Dimethylsulfoniopropionate in the Bohai and Yellow Seas

“…Clade_ I SAR11 ( α‐Proteobacteria ) was correlated with DLA and bacterial abundance, and Thioglobaceae ( γ‐Proteobacteria ) abundance was correlated with DMSP d,p concentrations (Figure S4 in Supporting Information ). The SAR11 clade, which was the most dominant bacterial group (18 ± 2.1%), may be a significant contributor of DMS in Australian coastal shelf waters (O'Brien et al., 2022). The SAR11 clade was the most abundant marine bacterial group and utilizes DMSP as a main sulfur source (Tripp et al., 2008).…”

“…DMS/DMSP concentrations are affected by phytoplankton and zooplankton species composition, zooplankton grazing, microbial consumption, and abiotic factors (McParland & Levine, 2019; O'Brien et al., 2022; Stefels et al., 2007; Yu et al., 2021). Our study analyzed the relationship between the distribution of DMS/DMSP d,p and biological factors and provides a more comprehensive understanding of the factors controlling DMS/DMSP concentrations.…”

“…DMSP cleavage enzymes originate from bacteria and phytoplankton (Steinke et al, 2003). O'Brien et al (2022) showed that phytoplankton DLA and bacterial DLA are significantly correlated with the DMS concentration in Australian coastal shelf waters. Previous observations have shown a strong positive relationship between DLA and dominant phytoplankton taxa.…”

“…Many studies have focused on the temporal and spatial distributions and transformation of DMS and DMSP in the surface seawater and the sea‐to‐air exchange, as well as the effects of some environmental factors on these sulfur compounds (Jackson & Gabric, 2022; Kiene, 1992; O'Brien et al., 2022; Owen et al., 2021; Shemi et al., 2021; Yang et al., 2011; Yu et al., 2021). The Bohai Sea (BS) and Yellow Sea (YS) are marginal seas located in the western Pacific Ocean that comprise a total area of 460,000 km 2 (Chen et al., 2022).…”