DMSP Production by Coral-Associated Bacteria
Dimethylsulfoniopropionate (DMSP) is an important molecule in the marine sulfur cycle, produced in large amounts by corals and their dinoflagellate endosymbionts, Symbiodiniaceae. Although corals are known to harbour bacteria that can catabolise DMSP, the recent discovery of bacteria capable of prod...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-05-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2022.869574/full |
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| author | Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Cherie A. Motti Cherie A. Motti Jia Zhang Jia Zhang Ira R. Cooke Ira R. Cooke Jonathan D. Todd David J. Miller David J. Miller David J. Miller David G. Bourne David G. Bourne David G. Bourne Jean-Baptiste Raina |
| author_facet | Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Cherie A. Motti Cherie A. Motti Jia Zhang Jia Zhang Ira R. Cooke Ira R. Cooke Jonathan D. Todd David J. Miller David J. Miller David J. Miller David G. Bourne David G. Bourne David G. Bourne Jean-Baptiste Raina |
| author_sort | Felicity W.I. Kuek |
| collection | DOAJ |
| description | Dimethylsulfoniopropionate (DMSP) is an important molecule in the marine sulfur cycle, produced in large amounts by corals and their dinoflagellate endosymbionts, Symbiodiniaceae. Although corals are known to harbour bacteria that can catabolise DMSP, the recent discovery of bacteria capable of producing DMSP in coastal and deep-sea environments raises the possibility of a bacterial contribution to the DMSP output of corals. Here, 157 bacteria associated with four common coral species were isolated and screened for their ability to produce DMSP by targeting dsyB, a key gene involved in DMSP biosynthesis. Approximately 9% (14 out of 157) of the bacterial isolates harboured dsyB, all being members of the Alphaproteobacteria. The ability of these isolates to produce DMSP was confirmed by liquid chromatography-mass spectrometry (LC-MS) and nuclear magnetic resonance (NMR) measurements. A dsyB-harbouring strain, Shimia aestuarii AMM-P-2, was selected for genome sequencing. This strain harbours the complete genetic machinery to (i) assimilate sulfate and synthesise the DMSP precursors, cysteine and methionine; (ii) demethylate DMSP and generate methanethiol; (iii) cleave DMSP, generating dimethyl sulfide (DMS) and acrylate; and (iv) utilise or detoxify acrylate. The impacts of varied environmental factors (temperature, salinity, light and UV radiation) on S. aestuarii AMM-P-2 DMSP biosynthesis were characterised. DMSP levels in S. aestuarii AMM-P-2 increased almost two-fold under both hypersaline conditions (40 PSU) and high UV exposure. DMSP catabolism through the cleavage pathway also increased under these conditions, producing the antioxidants DMS and acrylate, a potential response to the oxidative stress generated. Overall, our results reveal that coral-associated bacteria can synthesize DMSP and may therefore contribute to DMSP production by the coral holobiont. |
| first_indexed | 2024-12-12T22:11:45Z |
| format | Article |
| id | doaj.art-5222a15cd5f74c0a9f88a8d9236c27fe |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-12-12T22:11:45Z |
| publishDate | 2022-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-5222a15cd5f74c0a9f88a8d9236c27fe2022-12-22T00:10:13ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-05-01910.3389/fmars.2022.869574869574DMSP Production by Coral-Associated BacteriaFelicity W.I. Kuek0Felicity W.I. Kuek1Felicity W.I. Kuek2Felicity W.I. Kuek3Felicity W.I. Kuek4Cherie A. Motti5Cherie A. Motti6Jia Zhang7Jia Zhang8Ira R. Cooke9Ira R. Cooke10Jonathan D. Todd11David J. Miller12David J. Miller13David J. Miller14David G. Bourne15David G. Bourne16David G. Bourne17Jean-Baptiste Raina18AIMS@JCU, Division of Research and Innovation, James Cook University, Townsville, QLD, AustraliaAustralian Research Council (ARC) Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, AustraliaCentre for Tropical Bioinformatics and Molecular Biology, James Cook University, Townsville, QLD, AustraliaCollege of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, QLD, AustraliaTropical Marine Water Quality and Impacts, Australian Institute of Marine Science, Townsville, QLD, AustraliaAIMS@JCU, Division of Research and Innovation, James Cook University, Townsville, QLD, AustraliaTropical Marine Water Quality and Impacts, Australian Institute of Marine Science, Townsville, QLD, AustraliaCentre for Tropical Bioinformatics and Molecular Biology, James Cook University, Townsville, QLD, AustraliaCollege of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, QLD, AustraliaCentre for Tropical Bioinformatics and Molecular Biology, James Cook University, Townsville, QLD, AustraliaCollege of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, QLD, AustraliaSchool of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, United KingdomAustralian Research Council (ARC) Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, AustraliaCentre for Tropical Bioinformatics and Molecular Biology, James Cook University, Townsville, QLD, AustraliaCollege of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, QLD, AustraliaAIMS@JCU, Division of Research and Innovation, James Cook University, Townsville, QLD, AustraliaTropical Marine Water Quality and Impacts, Australian Institute of Marine Science, Townsville, QLD, AustraliaCollege of Science and Engineering, James Cook University, Townsville, QLD, AustraliaClimate Change Cluster (C3), University of Technology Sydney, Ultimo, NSW, AustraliaDimethylsulfoniopropionate (DMSP) is an important molecule in the marine sulfur cycle, produced in large amounts by corals and their dinoflagellate endosymbionts, Symbiodiniaceae. Although corals are known to harbour bacteria that can catabolise DMSP, the recent discovery of bacteria capable of producing DMSP in coastal and deep-sea environments raises the possibility of a bacterial contribution to the DMSP output of corals. Here, 157 bacteria associated with four common coral species were isolated and screened for their ability to produce DMSP by targeting dsyB, a key gene involved in DMSP biosynthesis. Approximately 9% (14 out of 157) of the bacterial isolates harboured dsyB, all being members of the Alphaproteobacteria. The ability of these isolates to produce DMSP was confirmed by liquid chromatography-mass spectrometry (LC-MS) and nuclear magnetic resonance (NMR) measurements. A dsyB-harbouring strain, Shimia aestuarii AMM-P-2, was selected for genome sequencing. This strain harbours the complete genetic machinery to (i) assimilate sulfate and synthesise the DMSP precursors, cysteine and methionine; (ii) demethylate DMSP and generate methanethiol; (iii) cleave DMSP, generating dimethyl sulfide (DMS) and acrylate; and (iv) utilise or detoxify acrylate. The impacts of varied environmental factors (temperature, salinity, light and UV radiation) on S. aestuarii AMM-P-2 DMSP biosynthesis were characterised. DMSP levels in S. aestuarii AMM-P-2 increased almost two-fold under both hypersaline conditions (40 PSU) and high UV exposure. DMSP catabolism through the cleavage pathway also increased under these conditions, producing the antioxidants DMS and acrylate, a potential response to the oxidative stress generated. Overall, our results reveal that coral-associated bacteria can synthesize DMSP and may therefore contribute to DMSP production by the coral holobiont.https://www.frontiersin.org/articles/10.3389/fmars.2022.869574/fullDMSPsulfur cyclecoral-associated bacteriaholobiontacrylate |
| spellingShingle | Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Felicity W.I. Kuek Cherie A. Motti Cherie A. Motti Jia Zhang Jia Zhang Ira R. Cooke Ira R. Cooke Jonathan D. Todd David J. Miller David J. Miller David J. Miller David G. Bourne David G. Bourne David G. Bourne Jean-Baptiste Raina DMSP Production by Coral-Associated Bacteria Frontiers in Marine Science DMSP sulfur cycle coral-associated bacteria holobiont acrylate |
| title | DMSP Production by Coral-Associated Bacteria |
| title_full | DMSP Production by Coral-Associated Bacteria |
| title_fullStr | DMSP Production by Coral-Associated Bacteria |
| title_full_unstemmed | DMSP Production by Coral-Associated Bacteria |
| title_short | DMSP Production by Coral-Associated Bacteria |
| title_sort | dmsp production by coral associated bacteria |
| topic | DMSP sulfur cycle coral-associated bacteria holobiont acrylate |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2022.869574/full |
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