The rapid turnover of dimethylsulfoniopropionate (DMSP), likely the most relevant dissolved organic sulfur compound in the surface ocean, makes it pivotal to understand the cycling of organic sulfur. Dimethylsulfoniopropionate is mainly synthesized by phytoplankton, and it can be utilized as carbon and sulfur sources by marine bacteria or cleaved by bacteria or algae to produce the volatile compound dimethylsulfide (DMS), involved in the formation of sulfate aerosols. The fluxes between the consumption (i.e., demethylation) and cleavage pathways are thought to depend on community interactions and their sulfur demand. However, a quantitative assessment of the sulfur partitioning between each of these pathways is still missing. Here, we report for the first time the sulfur isotope fractionations by enzymes involved in DMSP degradation with different catalytic mechanisms, expressed heterologously in
Sulfur metabolites that facilitate oceanic phytoplankton–bacteria carbon flux
Unlike biologically available nitrogen and phosphorus, which are often at limiting concentrations in surface seawater, sulfur in the form of sulfate is plentiful and not considered to constrain marine microbial activity. Nonetheless, in a model system in which a marine bacterium obtains all of its carbon from co-cultured phytoplankton, bacterial gene expression suggests that at least seven dissolved organic sulfur (DOS) metabolites support bacterial heterotrophy. These labile exometabolites of marine dinoflagellates and diatoms include taurine, N-acetyltaurine, isethionate, choline-O-sulfate, cysteate, 2,3-dihydroxypropane-1-sulfonate (DHPS), and dimethylsulfoniopropionate (DMSP). Leveraging from the compounds identified in this model system, we assessed the role of sulfur metabolites in the ocean carbon cycle by mining the Tara Oceans dataset for diagnostic genes. In the 1.4 million bacterial genome equivalents surveyed, estimates of the frequency of genomes harboring the capability for DOS metabolite utilization ranged broadly, from only 1 out of every 190 genomes (for the C2 sulfonate isethionate) to 1 out of every 5 (for the sulfonium compound DMSP). Bacteria able to participate in DOS transformations are dominated by Alphaproteobacteria in the surface ocean, but by SAR324, Acidimicrobiia, and Gammaproteobacteria at mesopelagic depths, where the capability for utilization occurs in higher frequency than in surface bacteria for more than half the sulfur metabolites. The discovery of an abundant and diverse suite of marine bacteria with the genetic capacity for DOS transformation argues for an important role for sulfur metabolites in the pelagic ocean carbon cycle.
more » « less- Award ID(s):
- 1656311
- NSF-PAR ID:
- 10485628
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 13
- Issue:
- 10
- ISSN:
- 1751-7362
- Format(s):
- Medium: X Size: p. 2536-2550
- Size(s):
- ["p. 2536-2550"]
- Sponsoring Org:
- National Science Foundation
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Abstract Escherichia coli . We show that the residual DMSP from the demethylation pathway is 2.7‰ enriched inδ 34S relative to the initial DMSP, and that the fractionation factor (34ε ) of the cleavage pathways varies between −1 and −9‰. The incorporation of these fractionation factors into mass balance calculations constrains the biological fates of DMSP in seawater, supports the notion that demethylation dominates over cleavage in marine environments, and could be used as a proxy for the dominant pathways of degradation of DMSP by marine microbial communities. -
null (Ed.)Abstract. Temperature is a master parameter in the marine carbon cycle, exerting a critical control on the rate of biological transformation of a variety of solid and dissolved reactants and substrates. Although in the construction of numerical models of marine carbon cycling, temperature has been long recognised as a key parameter in the production and export of organic matter at the ocean surface, its role in the ocean interior is much less frequently accounted for. There, bacteria (primarily) transform sinking particulate organic matter (POM) into its dissolved constituents and consume dissolved oxygen (and/or other electron acceptors such as sulfate). The nutrients and carbon thereby released then become available for transport back to the surface, influencing biological productivity and atmospheric pCO2, respectively. Given the substantial changes in ocean temperature occurring in the past, as well as in light of current anthropogenic warming, appropriately accounting for the role of temperature in marine carbon cycling may be critical to correctly projecting changes in ocean deoxygenation and the strength of feedbacks on atmosphericpCO2. Here we extend and calibrate a temperature-dependent representation ofmarine carbon cycling in the cGENIE.muffin Earth system model, intended forboth past and future climate applications. In this, we combine atemperature-dependent remineralisation scheme for sinking organic matterwith a biological export production scheme that also includes a dependenceon ambient seawater temperature. Via a parameter ensemble, we jointlycalibrate the two parameterisations by statistically contrasting model-projected fields of nutrients, oxygen, and the stable carbon isotopicsignature (δ13C) of dissolved inorganic carbon in the oceanwith modern observations. We additionally explore the role of temperature inthe creation and recycling of dissolved organic matter (DOM) and hence itsimpact on global carbon cycle dynamics. We find that for the present day, the temperature-dependent version showsa fit to the data that is as good as or better than the existing tuned non-temperature-dependent version of the cGENIE.muffin. The main impact ofaccounting for temperature-dependent remineralisation of POM is in drivinghigher rates of remineralisation in warmer waters, in turn driving a morerapid return of nutrients to the surface and thereby stimulating organicmatter production. As a result, more POM is exported below 80 m but onaverage reaches shallower depths in middle- and low-latitude warmer waterscompared to the standard model. Conversely, at higher latitudes, colderwater temperature reduces the rate of nutrient resupply to the surface andPOM reaches greater depth on average as a result of slower subsurface ratesof remineralisation. Further adding temperature-dependent DOM processeschanges this overall picture only a little, with a slight weakening ofexport production at higher latitudes. As an illustrative application of the new model configuration andcalibration, we take the example of historical warming and briefly assessthe implications for global carbon cycling of accounting for a more completeset of temperature-dependent processes in the ocean. We find that betweenthe pre-industrial era (ca. 1700) and the present (year 2010), in response to asimulated air temperature increase of 0.9 ∘C and an associatedprojected mean ocean warming of 0.12 ∘C (0.6 ∘C insurface waters and 0.02 ∘C in deep waters), a reduction inparticulate organic carbon (POC) export at 80 m of just 0.3 % occurs (or 0.7 % including a temperature-dependent DOM response). However, due to this increased recycling nearer the surface, the efficiency of the transfer of carbon away from the surface (at 80 m) to the deep ocean (at 1040 m) is reduced by 5 %. In contrast, with no assumed temperature-dependent processes impacting production or remineralisation of either POM or DOM, global POC export at 80 m falls by 2.9 % between the pre-industrial era and the present day as a consequence of ocean stratification and reduced nutrient resupply to the surface. Our analysis suggests that increased temperature-dependent nutrient recycling in the upper ocean has offset much of the stratification-induced restriction in its physical transport.more » « less
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