Dataset Information

Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP).

ABSTRACT: Dominant coral-associated Endozoicomonas bacteria species are hypothesized to play a role in the coral sulfur cycle by metabolizing dimethylsulfoniopropionate (DMSP) into dimethylsulfide (DMS); however, no sequenced genome to date harbors genes for this process. In this study, we assembled high-quality (>95% complete) draft genomes of strains of the recently added species Endozoicomonas acroporae (Acr-14T, Acr-1, and Acr-5) isolated from the coral Acropora sp. and performed a comparative genomic analysis on the genus Endozoicomonas. We identified DMSP CoA-transferase/lyase-a dddD gene homolog in all sequenced genomes of E. acroporae strains-and functionally characterized bacteria capable of metabolizing DMSP into DMS via the DddD cleavage pathway using RT-qPCR and gas chromatography (GC). Furthermore, we demonstrated that E. acroporae strains can use DMSP as a carbon source and have genes arranged in an operon-like manner to link DMSP metabolism to the central carbon cycle. This study confirms the role of Endozoicomonas in the coral sulfur cycle.

SUBMITTER: Tandon K

PROVIDER: S-EPMC7174347 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP).

Tandon Kshitij K Lu Chih-Ying CY Chiang Pei-Wen PW Wada Naohisa N Yang Shan-Hua SH Chan Ya-Fan YF Chen Ping-Yun PY Chang Hsiao-Yu HY Chiou Yu-Jing YJ Chou Ming-Shean MS Chen Wen-Ming WM Tang Sen-Lin SL

The ISME journal 20200213 5

Dominant coral-associated Endozoicomonas bacteria species are hypothesized to play a role in the coral sulfur cycle by metabolizing dimethylsulfoniopropionate (DMSP) into dimethylsulfide (DMS); however, no sequenced genome to date harbors genes for this process. In this study, we assembled high-quality (>95% complete) draft genomes of strains of the recently added species Endozoicomonas acroporae (Acr-14<sup>T</sup>, Acr-1, and Acr-5) isolated from the coral Acropora sp. and performed a comparat ...[more]

PMID: 32055028

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Project description:Dimethylsulfoniopropionate (DMSP), a key component of the global geochemical sulfur cycle, is a secondary metabolite produced in large quantities by marine phytoplankton and utilized as an osmoprotectant, thermoprotectant and antioxidant. Marine bacteria can use two pathways to degrade and catabolize DMSP, a demethylation pathway and a cleavage pathway that produces the climate active gas dimethylsulfide (DMS). Whether marine bacteria can also accumulate DMSP as an osmoprotectant to maintain the turgor pressure of the cell in response to changes in external osmolarity has received little attention. The marine halophile Vibrio parahaemolyticus, contains at least six osmolyte transporters, four betaine carnitine choline transport (BCCT) carriers BccT1-BccT4 and two ABC-family ProU transporters. In this study, we showed that DMSP is used as an osmoprotectant by V. parahaemolyticus and several other Vibrio species including V. cholerae and V. vulnificus Using a V. parahaemolyticus proU double mutant, we demonstrated that these ABC transporters are not required for DMSP uptake. However, a bccT null mutant lacking all four BCCTs had a growth defect compared to wild type in high salinity media supplemented with DMSP. Using mutants possessing only one functional BCCT in growth pattern assays, we identified two BCCT-family transporters, BccT1 and BccT2, which are carriers of DMSP. The only V. parahaemolyticus BccT homolog that V. cholerae and V. vulnificus possess is BccT3 and functional complementation in Escherichia coli MKH13 showed V. cholerae VcBccT3 could transport DMSP. In V. vulnificus strains, we identified and characterized an additional BCCT family transporter, which we named BccT5 that was also a carrier for DMSP.Importance DMSP is present in the marine environment, produced in large quantities by marine phytoplankton as an osmoprotectant, and is an important component of the global geochemical sulfur cycle. This algal osmolyte has not been previously investigated for its role in marine heterotrophic bacterial osmotic stress response. Vibrionaceae are marine species, many of which are halophiles exemplified by V. parahaemolyticus, a species that possesses at least six transporters for the uptake of osmolytes. Here, we demonstrated that V. parahaemolyticus and other Vibrio species can accumulate DMSP as an osmoprotectant and show that several BCCT family transporters uptake DMSP. These studies suggest that DMSP is a significant bacterial osmoprotectant, which may be important for understanding the fate of DMSP in the environment. DMSP is produced and present in coral mucus and Vibrio species form part of the microbial communities associated with them. The function of DMSP in these interactions is unclear, but could be an important driver for these associations allowing Vibrio proliferation. This work suggests that DMSP likely has an important role in heterotrophic bacteria ecology than previously appreciated.

Dataset Information

Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP).

Publications

Comparative genomics: Dominant coral-bacterium Endozoicomonas acroporae metabolizes dimethylsulfoniopropionate (DMSP).

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