The osmolyte ties that bind: genomic insights into synthesis and breakdown of organic osmolytes in marine microbes

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in McParland, E. L., Alexander, H., & Johnson, W. M. The osmolyte ties that bind: genomic insights into synthesis and breakdown of organic osmolytes in marine microbes. Frontiers in Marine Science, 8, (2021): 689306, https://doi.org/10.3389/fmars.2021.689306.The production and consumption of organic matter by marine organisms plays a central role in the marine carbon cycle. Labile organic compounds (metabolites) are the major currency of energetic demands and organismal interaction, but these compounds remain elusive because of their rapid turnover and concomitant minuscule concentrations in the dissolved organic matter pool. Organic osmolytes are a group of small metabolites synthesized at high intracellular concentrations (mM) to regulate cellular osmolarity and have the potential to be released as abundant dissolved substrates. Osmolytes may represent an essential currency of exchange among heterotrophic prokaryotes and primary and secondary producers in marine food webs. For example, the well-known metabolite dimethylsulfoniopropionate (DMSP) is used as an osmolyte by some phytoplankton and can be subsequently metabolized by 60% of the marine bacterial community, supplying up to 13% of the bacterial carbon demand and 100% of the bacterial sulfur demand. While marine osmolytes have been studied for decades, our understanding of their cycling and significance within microbial communities is still far from comprehensive. Here, we surveyed the genes responsible for synthesis, breakdown, and transport of 14 key osmolytes. We systematically searched for these genes across marine bacterial genomes (n = 897) and protistan transcriptomes (n = 652) using homologous protein profiles to investigate the potential for osmolyte metabolisms. Using the pattern of gene presence and absence, we infer the metabolic potential of surveyed microbes to interact with each osmolyte. Specifically, we identify: (1) complete pathways for osmolyte synthesis in both prokaryotic and eukaryotic marine microbes, (2) microbes capable of transporting osmolytes but lacking complete synthesis and/or breakdown pathways, and (3) osmolytes whose synthesis and/or breakdown appears to be specialized and is limited to a subset of organisms. The analysis clearly demonstrates that the marine microbial loop has the genetic potential to actively recycle osmolytes and that this abundant group of small metabolites may function as a significant source of nutrients through exchange among diverse microbial groups that significantly contribute to the cycling of labile carbon.EM was supported by the Postdoctoral Scholar Program at Woods Hole Oceanographic Institution. WJ was supported by a Research Initiative Award from the College of Arts and Sciences at the University of North Carolina Wilmington. HA was supported by a Independent Research and Development Award from the Woods Hole Oceanographic Institution

The microbiological drivers of temporally dynamic Dimethylsulfoniopropionate cycling processes in Australian coastal shelf waters

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in O’Brien, J., McParland, E. L., Bramucci, A. R., Ostrowski, M., Siboni, N., Ingleton, T., Brown, M. V., Levine, N. M., Laverock, B., Petrou, K., & Seymour, J. The microbiological drivers of temporally dynamic Dimethylsulfoniopropionate cycling processes in Australian coastal shelf waters. Frontiers in Microbiology, 13, (2022): 894026, https://doi.org/10.3389/fmicb.2022.894026.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.This research was supported by the Australian Research Council Grants FT130100218 and DP180100838 awarded to JS and DP140101045 awarded to JS and KP, as well as an Australian Government Research Training Program Scholarship awarded to JO’B

Parameterizing the impact of seawater temperature and irradiance on dimethylsulfide (DMS) in the Great Barrier Reef and the contribution of coral reefs to the global sulfur cycle

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Jackson, R. L., Gabric, A. J., Matrai, P. A., Woodhouse, M. T., Cropp, R., Jones, G. B., Deschaseaux, E. S. M., Omori, Y., McParland, E. L., Swan, H. B., & Tanimoto, H. Parameterizing the impact of seawater temperature and irradiance on dimethylsulfide (DMS) in the Great Barrier Reef and the contribution of coral reefs to the global sulfur cycle. Journal of Geophysical Research:Oceans, 126(3), (2021): e2020JC016783, https://doi.org/10.1029/2020JC016783.Biogenic emissions of dimethylsulfide (DMS) are an important source of sulfur to the atmosphere, with implications for aerosol formation and cloud albedo over the ocean. Natural aerosol sources constitute the largest uncertainty in estimates of aerosol radiative forcing and climate and thus, an improved understanding of DMS sources is needed. Coral reefs are strong point sources of DMS; however, this coral source of biogenic sulfur is not explicitly included in climatologies or in model simulations. Consequently, the role of coral reefs in local and regional climate remains uncertain. We aim to improve the representation of tropical coral reefs in DMS databases by calculating a climatology of seawater DMS concentration (DMSw) and sea-air flux in the Great Barrier Reef (GBR), Australia. DMSw is calculated from remotely sensed observations of sea surface temperature and photosynthetically active radiation using a multiple linear regression model derived from field observations of DMSw in the GBR. We estimate that coral reefs and lagoon waters in the GBR (∼347,000 km2) release 0.03–0.05 Tg yr−1 of DMS (0.02 Tg yr−1 of sulfur). Based on this estimate, global tropical coral reefs (∼600,000 km2) could emit 0.08 Tg yr−1 of DMS (0.04 Tg yr−1 of sulfur), with the potential to influence the local radiative balance.Australian Research Council. Grant Number: DP150101649 National Science Foundation (NSF). Grant Number: 1543450 Ministry of Education, Culture, Sports, Science and Technology Grants-in-Aid for Scientific Research. Grant Number: 23310016,16H02967,24241010,15H01732 Ministry of Education, Culture, Sports, Science and Technology Grant-in-Aid for Young Scientists. Grant Number: 17K1281

Biogeographical and seasonal dynamics of the marine Roseobacter community and ecological links to DMSP-producing phytoplankton

Abstract Ecological interactions between marine bacteria and phytoplankton play a pivotal role in governing the ocean’s major biogeochemical cycles. Among these, members of the marine Roseobacter Group (MRG) can establish mutualistic relationships with phytoplankton that are, in part, maintained by exchanges of the organosulfur compound, dimethylsulfoniopropionate (DMSP). Yet most of what is known about these interactions has been derived from culture-based laboratory studies. To investigate temporal and spatial co-occurrence patterns between members of the MRG and DMSP-producing phytoplankton we analysed 16S and 18S rRNA gene amplicon sequence variants (ASVs) derived from 5 years of monthly samples from seven environmentally distinct Australian oceanographic time-series. The MRG and DMSP-producer communities often displayed contemporaneous seasonality, which was greater in subtropical and temperate environments compared to tropical environments. The relative abundance of both groups varied latitudinally, displaying a poleward increase, peaking (MRG at 33% of total bacteria, DMSP producers at 42% of eukaryotic phototrophs) during recurrent spring-summer phytoplankton blooms in the most temperate site (Maria Island, Tasmania). Network analysis identified 20,140 significant positive correlations between MRG ASVs and DMSP producers and revealed that MRGs exhibit significantly stronger correlations to high DMSP producers relative to other DMSP-degrading bacteria (Pelagibacter, SAR86 and Actinobacteria). By utilising the power of a continental network of oceanographic time-series, this study provides in situ confirmation of interactions found in laboratory studies and demonstrates that the ecological dynamics of an important group of marine bacteria are shaped by the production of an abundant and biogeochemically significant organosulfur compound