Dimethyl sulfide (DMS) is an organic sulfur gas which we all know as ‘the smell of the ocean’ and is emitted from seawater in massive amounts. It is produced by different marine life forms, from bacteria to algae and corals. Notable examples are SAR11, the most abundant bacteria in the ocean, and eukaryotic algae belonging to the haptophyte clade, such as Phaeocystis and the coccolithophore Emiliania. Those algae form immense blooms which are hotspots for DMS formation. Another key DMS producer is Symbiodinium, a symbiotic dinoflagellate that resides inside corals. Like algal blooms, coral reefs are hubs for DMS formation, which probably comes from three distinct biological origins - the bacteria in the coral mucus, the symbiotic dinoflagellate, and - intriguingly - the coral tissue itself, which is the only animal known to produce DMS.

DMS plays a key ecological role in marine food webs. Like us, many animals are sensitive to this pungent scent and can trace its source by swimming or flying over large distances. Seabirds were studied for this unique feature, as well as fish and even humpback whales. Thus, DMS acts as a signaling molecule - an ‘infochemical’, which carries valuable information: the presence of food. DMS emitted from algal blooms, for example, can lead top-predators to find dense planktonic populations that are associated with the blooming algae. Since most marine predators lack developed eyes, their sensitivity to chemotactic cues such as DMS is crucial for successful foraging and survival. This pro-grazing role of DMS was recently demonstrated for the direct consumers of algae as well, namely microzooplankton, which are mostly protists^1,2. This begs the question: why do algae produce large amounts of a smelly metabolite that attracts their predators and promotes their own death?

There are several hypotheses that can be tested to explain the paradoxical role of DMS in phytoplankton. For example, the protein producing DMS in the eukaryotic cells, a DMSP lyase enzyme³, may serve a vital role to promote cellular homeostasis during growth. Algae that live in the sunlit ocean are exposed to high oxidative stress from photosynthesis byproducts and UV radiation. The DMSP lyase enzyme was suggested to act as part of the cell’s antioxidant system, controlling the level of DMS and its precursor, dimethylsulfoniopropionate (DMSP), which are potent scavenges of reactive oxygen species. Yet proving the antioxidant hypothesis and other suggested cellular roles is a challenging task. Only a few algal DMSP lyase enzymes were isolated so far, which causes a major bottleneck to study this enzyme function. Among the algal species that are available in culture, we lack models that can be genetically transformed in order to learn about their gene function. Therefore, we must develop new model systems and experimental setups to understand why phytoplankton generate DMS in the ocean.

Our new paper in ISME Communications provides new bioinformatic tools to study the role of the DMSP lyase enzyme in your favorite algal model. We define unique sequence motifs in the DMSP lyase protein, which help us to detect the fingerprint of this enzyme in the genomes of distantly related taxa. So far, haptophytes and dinoflagellates were considered as the sole algal groups producing this gas, together with the green macroalga Ulva. With a set of criteria (the motifs, as well as the conservation of a racemase domain and active-site cysteine residues) we were able to define potential DMSP lyase homologs in several diatoms, green microalgae and others - significantly enlarging the phylogenetic tree of this enzyme. Importantly, several new species that are predicted to possess the DMSP lyase enzyme can be genetically transformed, which opens new opportunity for genetic studies on the DMSP lyase enzyme. We further analyzed the expression levels of the new DMSP lyase homologs in the Tara oceans dataset, a meta-transcriptomic project across the global ocean. High abundances of transcripts were associated to dinoflagellates, haptophytes, diatoms and others, with some possible links to environmental factors in specific ecological niches (such as nutrient availability). Expression of the DMSP lyase enzyme was even detected in the dark deep ocean by several mixotrophic dinoflagellates (which both eat prey and perform photosynthesis). This raises a new hypothesis about the involvement of DMS in mixotrophic metabolism in dinoflagellates.

So, for all phycologists and microbial ecologists out there - next time you’re having picnic on the beach, don’t forget to bring your laptop! Explore our dataset and you may find that your favorite phytoplankton potentially produces the wonderful smell of the ocean, via the activity of a mysterious DMSP lyase enzyme, or even a gene family of DMSP lyases! The study provides a suite of resources to start your journey, including manually curated sequences and in depth bioinformatic characterization. We hope to promote future experimentation in the lab and in the field, in the quest to find the cellular role of this ecologically important enzyme in marine phytoplankton.  

Read the full story here: Shemi, A., Ben-Dor, S., Rotkopf, R. et al. Phylogeny and biogeography of the algal DMS-releasing enzyme in the global ocean. ISME COMMUN. 3, 72 (2023). https://doi.org/10.1038/s43705-023-00280-2

References

1. Shemi A, et al., Dimethyl sulfide mediates microbial predator–prey interactions between zooplankton and algae in the ocean. Nat Microbiol. 2021.

2. Seymour J. et al., Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science. 2010.

3. Alcolombri U. et al., Identification of the algal dimethyl sulfide-releasing enzyme: A missing link in the marine sulfur cycle. Science. 2015.