MARINE MICROBIOLOGY

A day in the life of marine sulfonates

A Publisher Correction to this article was published on 18 October 2019

This article has been updated

Lab-based studies, combined with metatranscriptomic and metabolomic field analyses, reveal important diel-linked roles for sulfonates in the major classes of phytoplankton that produce them, and in the environment in which they feed ubiquitous heterotrophic bacteria.

Marine microbial nutrient cycling constitutes a vast and complex metabolic network in which photoautotrophs and heterotrophs intimately interact. Phytoplankton are vital to this network, generating a plethora of organic carbon molecules to levels approaching those made by terrestrial plants1. A significant portion of these are organosulfur molecules, representing up to 18,600 teragrams of oceanic sulfur2. Organosulfur molecules are beneficial to the organisms that produce them, and to the environment following their release, in which they stimulate chemotaxis, shape microbial communities and support the carbon, sulfur and energy requirements of heterotrophs3. The sheer diversity of the molecules and organisms involved in these processes has made deciphering interactions between marine photoautotrophs and heterotrophs challenging.

In this issue of Nature Microbiology, Durham and co-workers4 attempt to untangle some of these interactions by focusing on C2- and C3-sulfonates (compounds containing a carbon–sulfur bond (R–SO3)) (Fig. 1). Sulfonates constitute up to 95% of sulfur in terrestrial soil, being key microbial nutrient sources5. Recent work suggests that they are also important in the Earth’s oceans, with some diatoms containing millimolar levels of sulfonates, such as 2,3-dihydroxypropane-1-sulfonate (DHPS)6; Roseobacter species massively upregulating sulfonate transport and catabolism when co-cultured with diatoms7; and the genetic potential for sulfonate catabolism being abundant in surface ocean bacterial genomes8. The authors build on these findings by demonstrating that environmental sulfonate production is linked to diel cycling in the major classes of phytoplankton at levels that stimulate its import and catabolism by Earth’s most abundant heterotrophs.

Fig. 1: The proposed sulfonate metabolic network showing the diel cycle-linked production and release of sulfonates by many phytoplankton, and uptake by diverse heterotrophic bacteria.
figure1

a, Accumulation of five sulfonates (taurine, isethionate, DHPS, cysteate and sulfolactate) in phytoplankton during the daytime suggests that they may function in redox balancing and may also act as osmoprotectants. Phytoplankton sulfonate synthesis pathways were theorised on the presence of homologues to ratified sulfonate metabolic genes. Isethionate is derived from taurine through a taurine aminotransferase (encoded by tpa/toa) and sulfoacetaldehyde reductase (isfD), genes for which were detected in most phytoplankton (diatoms did not possess isfD). Taurine can be derived from cysteine through oxidation and decarboxylation steps, inferred by genes encoding putative cysteine dioxygenases (CDO1) and cysteine sulfinic acid decarboxylases (CSAD). Cysteate can be produced from serine through sulfonation reactions (SDH and PAPA-AS, encoding serine dehydratase and 3′-phosphoadenylyl sulfate:2-aminoacrylate C-sulfotransferase), and can be converted to taurine through decarboxylation via CSAD, or to sulfolactate via genes encoding cysteate aminotransferase (CoA) and sulfolactate dehydrogenase (comC). Hypothetical DHPS synthesis pathways from cysteate via cysteinolic acid, or via sulfolactate, were proposed without direct knowledge of the genes or enzymes involved. b, At night, a portion of the sulfonates are released from phytoplankton (by unconfirmed processes, for example, transport, lysis or leakage) and are imported by marine heterotrophic bacteria for catabolism to produce for example, acetyl-CoA, bisulfide and pyruvate, for carbon, energy and sulfur requirements. Questions arising on the genes involved in DHPS production, mutualistic exchange of molecules and chemotaxis are indicated by a question mark (?); C3-sulfonates are circled in green; C2-sulfonates are circled in orange; purely hypothetical reactions are indicated by dotted lines.

An impressive selection of phytoplankton and heterotrophic bacteria were screened for C2- and C3-sulfonates by targeted metabolomics (Fig. 1). Sulfonates were either undetected, for example, DHPS and isethionate, or present at low levels, typically less than one micromolar, in heterotrophic bacteria. In phytoplankon they were detected at higher levels in taxon-specific combinations; C2-sulfonates were widespread across the phytoplankton, whereas C3-sulfonates were more pronounced in diatoms and haptophytes, with DHPS reaching millimolar levels in most. This strongly supports globally abundant phytoplankton, not just diatoms, as the most likely source of marine sulfonates that feed diverse heterotrophs. Given the taxon-specific production of these sulfonates, they may be important in recruiting specific heterotrophs.

There are few mechanistic studies of phytoplankton sulfonate production9, and sulfonate synthetic pathways in these organisms are uncertain. The authors propose phytoplankton sulfonate metabolic pathways based on the presence of homologues to ratified sulfur metabolic genes (Fig. 1). Metabolism of cysteine and serine to taurine, and subsequently to isethionate, was predicted in most phytoplankton (Fig. 1). Interestingly, phytoplankton lacked the complete sulfoquinovose catabolic pathway, a ratified pathway for DHPS production10. Durham and co-workers propose well-reasoned alternative DHPS synthesis pathways, including the conversion of cysteate through sulfolactate to DHPS, or from cysteinolic acid9. These predicted pathways and candidate genes are plausible, but confirmation involving labelled substrates or enzyme characterization is still required. This is important given the conclusions stemming from the regulation of these genes in the environment and for future studies using them as reporters of environmental sulfonate synthesis.

Metabolomics and metatranscriptomics were used effectively on North Pacific samples to provide evidence that phytoplankton sulfate assimilation and sulfonate synthesis are coupled to diel rhythm, particularly in diatoms and haptophytes. Apart from the five identified sulfonates, 19 unknown sulfur-containing molecules were also detected, highlighting the need for studies on novel organosulfur molecules11. Alongside the diel-regulated sulfonates detected (isethionate, DHPS, taurine and, likely, cysteinolic acid), several sulfate assimilation and candidate sulfonate synthesis genes (for example, CDO1, SDH and CoA) displayed diel periodicity in diatoms and haptophytes. It will be interesting to see these findings confirmed in future pure culture studies. Completing the cycle, bacterial transcripts of ratified sulfonate catabolic genes8,12,13 were relatively abundant in bacterial metatranscriptomes from samples collected at dawn. Environmentally abundant SAR11, SAR116, Roseobacter and Gammaproteobacteria lineages (Fig. 1) were most active, and their sulfonate catabolic pathways were inferred for taurine, isethionate and/or DHPS, theoretically generating pyruvate, acetyl CoA or bisulfite for assimilation. Furthermore, the authors isolated a North Pacific SAR11 strain and showed that taurine and DHPS are effective carbon and energy sources, providing further evidence for the importance of phytoplankton-derived sulfonates in oceanic heterotroph productivity.

While sulfonates can accumulate to millimolar levels in some phytoplankton, we are left wondering why. Indeed, the same is true for other organosulfur molecules, for example, dimethylsulfoniopropionate (DMSP), which can accumulate to far higher intracellular concentrations in phytoplankton and has been the focus of numerous studies14. Like DMSP, some sulfonates are proposed to function as osmolytes15, and Durham and co-workers show that DHPS accumulation by Thalassiosira pseudonana is regulated by salinity alongside osmolytes, including DMSP and proline. It would be interesting to measure whether transcription of the proposed candidate sulfonate synthesis genes is regulated in the same way. The authors also posit that sulfonates may maintain redox balance during phototrophic metabolism. An important focus of future work should therefore be the ratification of candidate sulfonate synthesis genes and their mutation in model phytoplankton to establish their physiological effects. However, as many similar molecules accumulate to comparable (or higher) levels than sulfonates in, for example, diatoms, it may be difficult to discern a phenotype or role. Additionally, the localization of sulfonates and their synthetic enzymes within phytoplankton may help to infer their function as, for example, organelle-specific osmolytes16.

Finally, how do sulfonates end up in the oceans — through active export by phytoplankton, or from cell lysis or leakage? Do heterotrophs provide phytoplankton nutrients in return for their sulfonate treats — a similar situation to that described for some hormones and vitamins7,17? Do specific bacteria demonstrate chemotaxis towards sulfonates? This study has opened a window into these marine networks, and in doing so has provided plenty of avenues for future research.

Change history

  • 18 October 2019

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Correspondence to Jonathan D. Todd.

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Williams, B.T., Todd, J.D. A day in the life of marine sulfonates. Nat Microbiol 4, 1610–1611 (2019). https://doi.org/10.1038/s41564-019-0576-5

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