Dimethylsulfoniopropionate in corals and its interrelations with bacterial assemblages in coral surface mucus
P. R. Frade A B G , V. Schwaninger C , B. Glasl A , E. Sintes A , R. W. Hill D , R. Simó E and G. J. Herndl A FA University of Vienna, Department of Limnology and Bio-Oceanography, Althanstrasse 14, AT-1090 Vienna, Austria.
B Caribbean Research and Management of Biodiversity (CARMABI) Foundation, Piscaderabaai z/n, PO Box 2090, Willemstad, Curaçao.
C University of Innsbruck, Institute of Ecology, Technikerstrasse 25, AT-6020 Innsbruck, Austria.
D Michigan State University, Department of Zoology, 288 Farm Lane RM 203, East Lansing, MI 48824, USA.
E Institute of Marine Sciences (ICM-CSIC), Passeig Marítim de la Barceloneta 37-49, E-08003 Barcelona, Spain.
F Royal Netherlands Institute for Sea Research (NIOZ), Department of Biological Oceanography, 1790 AB Den Burg, Netherlands.
G Corresponding author. Email: pedro.rodrigues.frade@univie.ac.at
Environmental Chemistry 13(2) 252-265 https://doi.org/10.1071/EN15023
Submitted: 24 January 2015 Accepted: 3 April 2015 Published: 27 August 2015
Journal Compilation © CSIRO Publishing 2016 Open Access CC BY-NC-ND
Environmental context. Corals produce copious amounts of dimethylsulfoniopropionate (DMSP), a sulfur compound implicated in climate regulation. We studied DMSP concentrations inside corals and unveiled the linkage between DMSP availability and the abundance of DMSP-degrading bacterial groups inhabiting the corals’ surface. Our findings suggest that DMSP mediates the interplay between corals and microbes, highlighting the importance of sulfur compounds for microbial processes in corals and for the resilience of coral reef ecosystems.
Abstract. Corals produce copious amounts of dimethylsulfoniopropionate (DMSP), a sulfur compound thought to play a role in structuring coral-associated bacterial communities. We tested the hypothesis that a linkage exists between DMSP availability in coral tissues and the community dynamics of bacteria in coral surface mucus. We determined DMSP concentrations in three coral species (Meandrina meandrites, Porites astreoides and Siderastrea siderea) at two sampling depths (5 and 25 m) and times of day (dawn and noon) at Curaçao, Southern Caribbean. DMSP concentration (4–409 nmol cm–2 coral surface) varied with host species-specific traits such as Symbiodinium cell abundance, but not with depth or time of sampling. Exposure of corals to air caused a doubling of their DMSP concentration. The phylogenetic affiliation of mucus-associated bacteria was examined by clone libraries targeting three main subclades of the bacterial DMSP demethylase gene (dmdA). dmdA gene abundance was determined by quantitative Polymerase Chain Reaction (qPCR) against a reference housekeeping gene (recA). Overall, a higher availability of DMSP corresponded to a lower relative abundance of the dmdA gene, but this pattern was not uniform across all host species or bacterial dmdA subclades, suggesting the existence of distinct DMSP microbial niches or varying dmdA DMSP affinities. This is the first study quantifying dmdA gene abundance in corals and linking related changes in the community dynamics of DMSP-degrading bacteria to DMSP availability. Our study suggests that DMSP mediates the regulation of microbes by the coral host and highlights the significance of sulfur compounds for microbial processes in coral reefs.
References
[1] R. Simó, Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol. Evol. 2001, 16, 287.| Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links.Crossref | GoogleScholarGoogle Scholar | 11369106PubMed |
[2] R. P. Kiene, L. J. Linn, J. A. Bruton, New and important roles for DMSP in marine microbial communities. J. Sea Res. 2000, 43, 209.
| New and important roles for DMSP in marine microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Wrtbw%3D&md5=789cb96d8406d5bbead908e442a540f1CAS |
[3] A. D. Broadbent, G. B. Jones, R. J. Jones, DMSP in corals and benthic algae from the Great Barrier Reef. Estuar. Coast. Shelf Sci. 2002, 55, 547.
| DMSP in corals and benthic algae from the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xot1Kmsbs%3D&md5=070e582236c54ed605e704f487a7d2d9CAS |
[4] R. W. Hill, J. W. H. Dacey, D. A. Krupp, Dimethylsulfoniopropionate in reef corals. Bull. Mar. Sci. 1995, 57, 489.
[5] G. B. Jones, M. A. J. Curran, A. D. Broadbent, Dimethylsulphide in the South Pacific, in Recent Advances in Marine Science and Technology ‘94: Sixth Pacific Congress on Marine Science and Technology (Eds O. Bellwood, H. Choat, N. Saxena) 1994. p. 183–190 (PACON International and James Cook University of North Queensland: Townsville, Qld).
[6] J. Stefels, Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Res. 2000, 43, 183.
| Physiological aspects of the production and conversion of DMSP in marine algae and higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Wrtb4%3D&md5=23897818cf9950bd364d15554611ea98CAS |
[7] J. B. Raina, D. M. Tapiolas, S. Foret, A. Lutz, D. Abrego, J. Ceh, F. O. Seneca, P. L. Clode, D. G. Bourne, B. L. Willis, C. A. Motti, DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 2013, 502, 677.
| DMSP biosynthesis by an animal and its role in coral thermal stress response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs12ksL%2FN&md5=54e55bace7bdd8180dd2edcf2cee3f33CAS | 24153189PubMed |
[8] P. R. Frade, P. Bongaerts, A. J. S. Winkelhagen, L. Tonk, R. P. M. Bak, In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host, and algal symbiont. Limnol. Oceanogr. 2008, 53, 2711.
| In situ photobiology of corals over large depth ranges: a multivariate analysis on the roles of environment, host, and algal symbiont.Crossref | GoogleScholarGoogle Scholar |
[9] D. Tchernov, M. Y. Gorbunov, C. de Vargas, S. N. Yadav, A. J. Milligan, M. Haggblom, P. G. Falkowski, Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl. Acad. Sci. USA 2004, 101, 13531.
| Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFeiu7k%3D&md5=e2d4f7f38233280a246d2834b5f8df38CAS | 15340154PubMed |
[10] K. L. Van Alstyne, P. Schupp, M. Slattery, The distribution of dimethylsulfoniopropionate in tropical Pacific coral reef invertebrates. Coral Reefs 2006, 25, 321.
| The distribution of dimethylsulfoniopropionate in tropical Pacific coral reef invertebrates.Crossref | GoogleScholarGoogle Scholar |
[11] C. R. Reisch, M. A. Moran, W. B. Whitman, Bacterial catabolism of dimethylsulfoniopropionate (DMSP). Front. Microbiol. 2011, 2, 172.
| Bacterial catabolism of dimethylsulfoniopropionate (DMSP).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvFWmtQ%3D%3D&md5=2a7361dbb94fc7c80ba7b2886bfdbf19CAS | 21886640PubMed |
[12] J. B. Raina, D. Tapiolas, B. L. Willis, D. G. Bourne, Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl. Environ. Microbiol. 2009, 75, 3492.
| Coral-associated bacteria and their role in the biogeochemical cycling of sulfur.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntlShu74%3D&md5=37f0d05badc8e1574e35f123606e5c60CAS | 19346350PubMed |
[13] S. M. Vallina, R. Simó, Strong relationship between DMS and the solar radiation dose over the global surface ocean. Science 2007, 315, 506.
| Strong relationship between DMS and the solar radiation dose over the global surface ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotFCisg%3D%3D&md5=89cd9bc46fb8728247c131f4a427b8cdCAS | 17255509PubMed |
[14] G. P. Ayers, J. L. Gras, Seasonal relationship between cloud condensation nuclei and aerosol methanesulfonate in marine air. Nature 1991, 353, 834.
| Seasonal relationship between cloud condensation nuclei and aerosol methanesulfonate in marine air.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmvVCjs7g%3D&md5=5bafdf56ff9a700e243d744f6d995e12CAS |
[15] A. R. J. Curson, M. J. Sullivan, J. D. Todd, A. W. B. Johnston, DddY, a periplasmic dimethylsulfoniopropionate lyase found in taxonomically diverse species of Proteobacteria. ISME J. 2011, 5, 1191.
| DddY, a periplasmic dimethylsulfoniopropionate lyase found in taxonomically diverse species of Proteobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvVaqsb0%3D&md5=97d019804bcf8b2321fb9a4d7eb5f217CAS |
[16] M. P. de Souza, D. C. Yoch, Purification and characterization of dimethylsulfoniopropionate lyase from an alcaligenes-like dimethyl sulfide-producing marine isolate. Appl. Environ. Microbiol. 1995, 61, 21.
| 1:CAS:528:DyaK2MXivValtb0%3D&md5=5b66324a297ac81e57c3b01bd9b4805dCAS | 16534905PubMed |
[17] R. P. Kiene, L. J. Linn, J. Gonzalez, M. A. Moran, J. A. Bruton, Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl. Environ. Microbiol. 1999, 65, 4549.
| 1:CAS:528:DyaK1MXms1Oitro%3D&md5=c0f9dc9c3f8951b78d1d03b07617b57dCAS | 10508088PubMed |
[18] R. P. Kiene, Production of methanethiol from dimethylsulfoniopropionate in marine surface waters. Mar. Chem. 1996, 54, 69.
| Production of methanethiol from dimethylsulfoniopropionate in marine surface waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsFags78%3D&md5=b888cca6a19388bf5c6208323717afcaCAS |
[19] E. C. Howard, J. R. Henriksen, A. Buchan, C. R. Reisch, H. Burgmann, R. Welsh, W. Ye, J. M. González, K. Mace, S. B. Joye, R. P. Kiene, W. B. Whitman, M. A. Moran, Bacterial taxa that limit sulfur flux from the ocean. Science 2006, 314, 649.
| Bacterial taxa that limit sulfur flux from the ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFeitr7M&md5=d02b3f54b8d92d215347f6b84a76dc59CAS | 17068264PubMed |
[20] E. C. Howard, S. Sun, E. J. Biers, M. A. Moran, Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ. Microbiol. 2008, 10, 2397.
| Abundant and diverse bacteria involved in DMSP degradation in marine surface waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFSksLvF&md5=b75790dff33d6b97cfc65d9c4ae98f90CAS | 18510552PubMed |
[21] J. B. Raina, E. A. Dinsdale, B. L. Willis, D. G. Bourne, Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol. 2010, 18, 101.
| Do the organic sulfur compounds DMSP and DMS drive coral microbial associations?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtVCksbs%3D&md5=bd9e73029ee5e8ff3fcd35a395a9f7feCAS | 20045332PubMed |
[22] M. Vila-Costa, R. Simó, H. Harada, J. M. Gasol, D. Slezak, R. P. Kiene, Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 2006, 314, 652.
| Dimethylsulfoniopropionate uptake by marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 17068265PubMed |
[23] D. T. Welsh, Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol. Rev. 2000, 24, 263.
| Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjslOru7Y%3D&md5=358a169cf656df1eccfdd8fb755def5fCAS | 10841973PubMed |
[24] J. R. Seymour, R. Simó, T. Ahmed, R. Stocker, Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 2010, 329, 342.
| Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosl2iu70%3D&md5=9160e8f0cec3e1f870bdb4bc1f5ff2baCAS | 20647471PubMed |
[25] M. Garren, K. Son, J. B. Raina, R. Rusconi, F. Menolascina, O. H. Shapiro, J. Tout, D. G. Bourne, J. R. Seymour, R. Stocker, A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J. 2014, 8, 999.
| A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvV2htbg%3D&md5=5b7327783a485908fcfa92b4b150727fCAS | 24335830PubMed |
[26] C. Evans, G. Malin, W. H. Wilson, P. S. Liss, Infectious titers of Emiliania huxleyi virus 86 are reduced by exposure to millimolar dimethyl sulfide and acrylic acid. Limnol. Oceanogr. 2006, 51, 2468.
| Infectious titers of Emiliania huxleyi virus 86 are reduced by exposure to millimolar dimethyl sulfide and acrylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOisr7I&md5=e9fa0d1d17c5f4e80e3ac2c27346784dCAS |
[27] W. Sunda, D. J. Kieber, R. P. Kiene, S. Huntsman, An antioxidant function for DMSP and DMS in marine algae. Nature 2002, 418, 317.
| An antioxidant function for DMSP and DMS in marine algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltlGms7k%3D&md5=1bcaa8d9ca44d13d4f343901c31cbed2CAS | 12124622PubMed |
[28] E. S. M. Deschaseaux, G. B. Jones, M. A. Deseo, K. M. Shepherd, R. P. Kiene, H. B. Swan, P. L. Harrison, B. D. Eyre, Effects of environmental factors on dimethylated sulfur compounds and their potential role in the antioxidant system of the coral holobiont. Limnol. Oceanogr. 2014, 59, 758.
| Effects of environmental factors on dimethylated sulfur compounds and their potential role in the antioxidant system of the coral holobiont.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVKjt7zE&md5=b1629dff25674b8132acc86857455f2aCAS |
[29] T. D. Ainsworth, R. V. Thurber, R. D. Gates, The future of coral reefs: a microbial perspective. Trends Ecol. Evol. 2010, 25, 233.
| The future of coral reefs: a microbial perspective.Crossref | GoogleScholarGoogle Scholar | 20006405PubMed |
[30] M. Garren, F. Azam, New method for counting bacteria associated with coral mucus. Appl. Environ. Microbiol. 2010, 76, 6128.
| New method for counting bacteria associated with coral mucus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlartr3L&md5=5d3ef122035d6ceee1b24291a6eff453CAS | 20656857PubMed |
[31] J. C. Bythell, C. Wild, Biology and ecology of coral mucus release. J. Exp. Mar. Biol. Ecol. 2011, 408, 88.
| Biology and ecology of coral mucus release.Crossref | GoogleScholarGoogle Scholar |
[32] M. E. Mouchka, I. Hewson, C. D. Harvell, Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr. Comp. Biol. 2010, 50, 662.
| Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts.Crossref | GoogleScholarGoogle Scholar | 21558231PubMed |
[33] A. D. Broadbent, G. B. Jones, DMS and DMSP in mucus ropes, coral mucus, surface films and sediment pore waters from coral reefs in the Great Barrier Reef. Mar. Freshwater Res. 2004, 55, 849.
| DMS and DMSP in mucus ropes, coral mucus, surface films and sediment pore waters from coral reefs in the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVens7jE&md5=74f3b38039bb5ef609d9ba545fa827e1CAS |
[34] R. P. M. Bak, Coral reefs and their zonation in the Netherlands Antilles. Stud. Geol. 1977, 4, 3.
[35] R. W. Hill, C. Li, A. D. Jones, J. P. Gunn, P. R. Frade, Abundant betaines in reef-building corals and ecological indicators of a photoprotective role. Coral Reefs 2010, 29, 869.
| Abundant betaines in reef-building corals and ecological indicators of a photoprotective role.Crossref | GoogleScholarGoogle Scholar |
[36] P. R. Frade, F. De Jongh, F. Vermeulen, J. Van Bleijswijk, R. P. M. Bak, Variation in symbiont distribution between closely related coral species over large depth ranges. Mol. Ecol. 2008, 17, 691.
| Variation in symbiont distribution between closely related coral species over large depth ranges.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXis1amtr0%3D&md5=7c45f6f75495e02cb597127ff04d8de0CAS | 18179427PubMed |
[37] C. Li, R. W. Hill, A. D. Jones, Determination of betaine metabolites and dimethylsulfoniopropionate in coral tissues using liquid chromatography-time-of-flight mass spectrometry and stable isotope-labeled internal standards. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2010, 878, 1809.
| Determination of betaine metabolites and dimethylsulfoniopropionate in coral tissues using liquid chromatography-time-of-flight mass spectrometry and stable isotope-labeled internal standards.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvV2qtLo%3D&md5=4956053263e5bfcdcd92be4dd66ed5d7CAS | 20627732PubMed |
[38] R. P. Kiene, D. Slezak, Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling. Limnol. Oceanogr. Methods 2006, 4, 80.
| Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlWnt70%3D&md5=d76bee9995b6021df822bbc9b36611e1CAS |
[39] R. Simó, Trace chromatographic analysis of dimethyl sulfoxide and related methylated sulfur compounds in natural waters. J. Chromatogr. A 1998, 807, 151.
| Trace chromatographic analysis of dimethyl sulfoxide and related methylated sulfur compounds in natural waters.Crossref | GoogleScholarGoogle Scholar | 9646493PubMed |
[40] R. P. Kiene, D. J. Kieber, D. Slezak, D. A. Toole, D. A. del Valle, J. Bisgrove, J. Brinkley, A. Rellinger, Distribution and cycling of dimethylsulfide, dimethylsulfoniopropionate, and dimethylsulfoxide during spring and early summer in the Southern Ocean south of New Zealand. Aquat. Sci. 2007, 69, 305.
| Distribution and cycling of dimethylsulfide, dimethylsulfoniopropionate, and dimethylsulfoxide during spring and early summer in the Southern Ocean south of New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ajtrvK&md5=eaf7594ad6cad129fb5e6c65bc81eab1CAS |
[41] J. A. Marsh, Primary productivity of reef-building calcareous red algae. Ecology 1970, 51, 255.
| Primary productivity of reef-building calcareous red algae.Crossref | GoogleScholarGoogle Scholar |
[42] V. A. Varaljay, E. C. Howard, S. Sun, M. A. Moran, Deep sequencing of a dimethylsulfoniopropionate-degrading gene (dmdA) by using PCR primer pairs designed on the basis of marine metagenomic data. Appl. Environ. Microbiol. 2010, 76, 609.
| Deep sequencing of a dimethylsulfoniopropionate-degrading gene (dmdA) by using PCR primer pairs designed on the basis of marine metagenomic data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVCitLc%3D&md5=016ce7a8dcf10fe9f58c6828e0e3d9f2CAS | 19948858PubMed |
[43] S. F. Altschul, T. L. Madden, A. A. Schaffer, J. H. Zhang, Z. Zhang, W. Miller, D. J. Lipman, Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25, 3389.
| Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFyhu7w%3D&md5=affae6d90453d87dde7d1ceee8ad38e5CAS | 9254694PubMed |
[44] M. Kearse, R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Meintjes, A. Drummond, Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012, 28, 1647.
| Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |
[45] G. W. Takle, I. K. Toth, M. B. Brurberg, Evaluation of reference genes for real-time RT-PCR expression studies in the plant pathogen Pectobacterium atrosepticum. BMC Plant Biol. 2007, 7, 50.
| Evaluation of reference genes for real-time RT-PCR expression studies in the plant pathogen Pectobacterium atrosepticum.Crossref | GoogleScholarGoogle Scholar | 17888160PubMed |
[46] D. E. Holmes, K. P. Nevin, D. R. Lovley, Comparison of 16S rRNA, nifD, recA, gyrB, rpoB and fusA genes within the family Geobacteraceae fam. nov. Int. J. Syst. Evol. Microbiol. 2004, 54, 1591.
| Comparison of 16S rRNA, nifD, recA, gyrB, rpoB and fusA genes within the family Geobacteraceae fam. nov.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVOlsb0%3D&md5=96d9c481fb271b620fd8ff030102ee4bCAS | 15388715PubMed |
[47] D. C. Montgomery, E. A. Peck, Introduction to Linear Regression Analysis, 2nd edn 1992 (Wiley: New York).
[48] M. P. Lesser, Exposure of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and inhibits photosynthesis. Limnol. Oceanogr. 1996, 41, 271.
| Exposure of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and inhibits photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjs1eru7k%3D&md5=abc6b0d26cb7ea3240e3926b6c3b3741CAS |
[49] G. B. Jones, E. Fischer, E. S. M. Deschaseaux, P. L. Harrison, The effect of coral bleaching on the cellular concentration of dimethylsulphoniopropionate in reef corals. J. Exp. Mar. Biol. Ecol. 2014, 460, 19.
| The effect of coral bleaching on the cellular concentration of dimethylsulphoniopropionate in reef corals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ensbzF&md5=d8a4bf603e1454ae99c8d59718611fcfCAS |
[50] D. M. Yost, R. J. Jones, C. L. Mitchelmore, Alterations in dimethylsulfoniopropionate (DMSP) levels in the coral Montastraea franksi in response to copper exposure. Aquat. Toxicol. 2010, 98, 367.
| Alterations in dimethylsulfoniopropionate (DMSP) levels in the coral Montastraea franksi in response to copper exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVegtrw%3D&md5=502040f60fd24146627d6c679dc01876CAS | 20378188PubMed |
[51] D. Slezak, G. J. Herndl, Effects of ultraviolet and visible radiation on the cellular concentrations of dimethylsulfoniopropionate (DMSP) in Emiliania huxleyi (strain L). Mar. Ecol. Prog. Ser. 2003, 246, 61.
| Effects of ultraviolet and visible radiation on the cellular concentrations of dimethylsulfoniopropionate (DMSP) in Emiliania huxleyi (strain L).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivVCjsLs%3D&md5=722f3b42da5bb8c59a44133ebd383b83CAS |
[52] T. C. LaJeunesse, G. Lambert, R. A. Andersen, M. A. Coffroth, D. W. Galbraith, Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. J. Phycol. 2005, 41, 880.
| Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCksLrI&md5=60fa7d03b23d9ad02be383c33aee4e5dCAS |
[53] D. W. Kemp, X. Hernandez-Pech, R. Iglesias-Prieto, W. K. Fitt, G. W. Schmidt, Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol. Oceanogr. 2014, 59, 788.
| Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVKjt73O&md5=f1a9c5c9cfc0a38006a2d2d8288c534eCAS |
[54] E. S. M. Deschaseaux, V. H. Beltran, G. B. Jones, M. A. Deseo, H. B. Swan, P. L. Harrison, B. D. Eyre, Comparative response of DMS and DMSP concentrations in Symbiodinium clades C1 and D1 under thermal stress. J. Exp. Mar. Biol. Ecol. 2014, 459, 181.
| Comparative response of DMS and DMSP concentrations in Symbiodinium clades C1 and D1 under thermal stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFWgtrnN&md5=bcbd28f2f69e9c1dc342c5f29eee514dCAS |
[55] P. Bongaerts, M. Carmichael, K. B. Hay, L. Tonk, P. R. Frade, O. Hoegh-Guldberg, Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. R. Soc. Open Sci. 2015, 2, 140297.
| Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species.Crossref | GoogleScholarGoogle Scholar | 26064597PubMed |
[56] D. M. Yost, C. L. Mitchelmore, Dimethylsulfoniopropionate (DMSP) lyase activity in different strains of the symbiotic alga Symbiodinium microadriaticum. Mar. Ecol. Prog. Ser. 2009, 386, 61.
| Dimethylsulfoniopropionate (DMSP) lyase activity in different strains of the symbiotic alga Symbiodinium microadriaticum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVClu7bO&md5=c662707482021a361c975f01e0c51842CAS |
[57] A. Salih, A. Larkum, G. Cox, M. Kuhl, O. Hoegh-Guldberg, Fluorescent pigments in corals are photoprotective. Nature 2000, 408, 850.
| Fluorescent pigments in corals are photoprotective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlaisA%3D%3D&md5=31381ba64e719c9244cffa9bfd3a601bCAS | 11130722PubMed |
[58] A. R. J. Curson, J. D. Todd, M. J. Sullivan, A. W. B. Johnston, Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat. Rev. Microbiol. 2011, 9, 849.
| Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12iurbE&md5=93732fa0bab3056569bbfa8e8bbadc36CAS |
[59] D. J. Schuller, C. R. Reisch, M. A. Moran, W. B. Whitman, W. N. Lanzilotta, Structures of dimethylsulfoniopropionate-dependent demethylase from the marine organism Pelagibacter ubique. Protein Sci. 2012, 21, 289.
| Structures of dimethylsulfoniopropionate-dependent demethylase from the marine organism Pelagibacter ubique.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpslyqsQ%3D%3D&md5=8e56a89f533016c100058bcb0e208ee0CAS | 22162093PubMed |
[60] E. C. Howard, S. L. Sun, C. R. Reisch, D. A. del Valle, H. Burgmann, R. P. Kiene, M. A. Moran, Changes in dimethylsulfoniopropionate demethylase gene assemblages in response to an induced phytoplankton bloom. Appl. Environ. Microbiol. 2011, 77, 524.
| Changes in dimethylsulfoniopropionate demethylase gene assemblages in response to an induced phytoplankton bloom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVOqsb0%3D&md5=25f4455694980de315d2dc8f65dab6c8CAS | 21097583PubMed |
[61] C. R. Reisch, M. A. Moran, W. B. Whitman, Dimethylsulfoniopropionate-dependent demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi. J. Bacteriol. 2008, 190, 8018.
| Dimethylsulfoniopropionate-dependent demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsV2lsLvK&md5=52fe46b2f71f5dd67a18921e4a0472bcCAS | 18849431PubMed |
[62] F. Rohwer, V. Seguritan, F. Azam, N. Knowlton, Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 2002, 243, 1.
| Diversity and distribution of coral-associated bacteria.Crossref | GoogleScholarGoogle Scholar |
[63] R. A. Littman, D. G. Bourne, B. L. Willis, Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host. Mol. Ecol. 2010, 19, 1978.
| Responses of coral-associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXns1Gitr8%3D&md5=9272a0005aa06e0cc7804317cf4fc7c0CAS | 20529072PubMed |
[64] M. Vila-Costa, J. M. Rinta-Kanto, R. S. Poretsky, S. Sun, R. P. Kiene, M. A. Moran, Microbial controls on DMSP degradation and DMS formation in the Sargasso Sea. Biogeochemistry 2014, 120, 295.
| Microbial controls on DMSP degradation and DMS formation in the Sargasso Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXptVCrt7w%3D&md5=c06c5016ec78fe5de34cd9368bdb6ab8CAS |
[65] M. S. Savoca, G. A. Nevitt, Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators. Proc. Natl. Acad. Sci. USA 2014, 111, 4157.
| Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtl2kt7w%3D&md5=935ded43fa889e5e490eb3ddb55b477eCAS | 24591607PubMed |