Smell the Sea: E. acroporae’s role in coral DMSP metabolism

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There is a smell that hits you as you approach a beach. It is tangy, and so closely tied to the beach or seaside that, were you to smell it in the winter, hundreds of miles from the coast, it would still bring to mind waves and sand. This aroma is the gas dimethylsulfide (DMS), made when a bacterium breaks down the sulfur compound dimethylsulfoniopropionate (DMSP) [1].

DMSP is one of the most abundant organosulfur compounds on our planet, and one billion tons of it are produced every year by marine phytoplankton, single-cell organisms, and coral-reefs [2, 3]. This DMSP from corals is not only a protectant against stress (osmotic and oxidative), but also an attractant for certain coral-associated bacterial groups [4, 5].

One of the most dominant and widely studied coral-associated bacterial groups belongs to the genus Endozoicomonas. The genus’ ecological functions have remained cryptic, but it has been hypothesized to play an active role in coral-sulfur metabolism, effectively metabolizing DMSP to DMS [6]. However, none of the sequenced genomes from coral isolates or other marine invertebrates harbor the gene(s) for this process.

In this study, we used cultures of the new species Endozoicomonas acroporae [7] from coral Acropora sp. and assembled high-quality draft genomes of its two new strains along with an earlier published type strain E. acroporae Acr-14T genome [8]. We profiled the abundance of E. acroporae across the Pacific Ocean and identified that this species has a broad host range and distribution. Using a comparative genomics approach, we identified a homolog of a DMSP acyl CoA-transferase/lyase gene, dddD, in all the E. acroporae strains. No other genes related to DMSP metabolism were found in any Endozoicomonas genomes. The functional activity of the dddD gene homolog was confirmed with qPCR and gas chromatography. Furthermore, we provide evidence that E. acroporae can grow on different concentrations of DMSP, and present an arrangement of genes in an operon-like manner that links DMSP metabolism to the central carbon cycle. This study provides the first genomic and functional evidence that Endozoicomonas plays a role in the coral sulfur cycle, putting an end to uncertainty around this genus’ place in the coral ecosystem.

You can read more about the work here: https://www.nature.com/articles/s41396-020-0610-x

Kshitij Tandon (First Author) and Transmission Electron Microscopy images and growth of E. acroporae strains (a) Acr-1 (b) Acr-5 and (c) Acr-14T at different concentrations of DMSP.

References

1.Johnston AWB, Todd JD, Sun L, Nikolaidou-Katsaridou MN, Curson ARJ, and Rogers R. Molecular diversity of bacterial production of the climate active gas, dimethylsulphide, a molecule that impinges on local and global symbioses. J. Exp. Bot. 2008:59;1059-1067.

2.Broadent AD, Jones GB, and Jones RJ. DMSP in Corals and Benthic Algae from the Great Barrier Reef.  Estuar. Coast. Shelf Sci. 2002:55;547-555.

3.Raina JB, Tapiolas DM, Foret S, Lutz A, Abrego D, Ceh J, et al. DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature. 2013:502;677-680.

4. Sunda W, Kieber DJ, Kiene RP, and Huntsman, S. An antioxidant function for DMSP and DMS in marine algae. Nature. 2002:418;317-320

5. Raina JB, Dinsdale EA, Willis BL, and Bourne DG. Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol. 2010:18;101-108.

6. Raina JB, Tapiolas D, Willis D, and Bourne DG. Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol. 2009:75;3492.

7. Sheu SY, Lin KR, Hsu MY, Sheu DS, Tang SL, et al. Endozoicomonas acroporae sp. nov. isolated from Acropora coral. Int. J. Syst. Evol. Microbiol. 2017:67;3791-3797.

8. Tandon K, Chiang PW, Chen WM, and Tang SL. Draft Genome Sequence of Endozoicomonas acroporae Strain Acr-14T, Isolated from Acropora Coral. Genome Announc. 2018;6(6):e0156-17.

Sen-Lin Tang

Research Fellow/Professor, Biodiversity Research Center, Academia Sinica

Metagenomics, aquatic microbial ecology, coral microbiota

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