Molecular diversity of bacterial production of the climate-changing gas, dimethyl sulphide, a molecule that impinges on local and global symbioses

Johnston, Andrew; Todd, Jonathan D.; Sun, Lina; Nikolaidou-Katsaridou, M. Nefeli; Curson, Andrew R. J.; Rogers, Rachel

doi:10.1093/jxb/erm264

Cited by 37 publications

(43 citation statements)

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“…The isolates derived from our coral samples were related to Photobacterium, Halomonas, and Shewanella spp., as well as to several Vibrio spp. Acrylic acid degradation has been recorded previously for Halomonas (24), and positive chemotactic responses to acrylic acid were observed for Vibrio (60). Vibrio-related organisms, known to be implicated in various coral diseases (64), were a major constituent of our coral libraries, representing up to 10% of the clones in the A. millepora mucus.…”

Section: Discussionsupporting

confidence: 58%

“…High concentrations of the organic sulfur compounds, DMSP and DMS, have previously been reported to be produced by dinoflagellates that are symbiotic with hard coral species, although the potential role of these compounds in structuring coral-associated microbial communities has not previously been investigated. The present study is the first to report the isolation of coral-associated bacteria that are capable of metabolizing DMSP and DMS organic sulfur compounds and, along with the study by Johnston et al (24), one of the first to isolate acrylic acid-degrading bacteria in general. The findings presented here support the hypothesis that by-products of coral algal photosynthesis, which exude high concentrations of DMSP and DMS, can support bacteria capable of metabolizing DMSP, DMS, and acrylic acid.…”

Section: Discussionsupporting

confidence: 54%

“…To date, only three studies have isolated bacteria involved in the metabolism of acrylic acid (2,24,71), highlighting a lack of knowledge in this area. The isolates derived from our coral samples were related to Photobacterium, Halomonas, and Shewanella spp., as well as to several Vibrio spp.…”

Section: Discussionmentioning

confidence: 99%

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Coral-Associated Bacteria and Their Role in the Biogeochemical Cycling of Sulfur

Raina

Tapiolas

Willis

et al. 2009

Appl Environ Microbiol

380

320

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Marine bacteria play a central role in the degradation of dimethylsulfoniopropionate (DMSP) to dimethyl sulfide (DMS) and acrylic acid, DMS being critical to cloud formation and thereby cooling effects on the climate. High concentrations of DMSP and DMS have been reported in scleractinian coral tissues although, to date, there have been no investigations into the influence of these organic sulfur compounds on coralassociated bacteria. Two coral species, Montipora aequituberculata and Acropora millepora, were sampled and their bacterial communities were characterized by both culture-dependent and molecular techniques. Four genera, Roseobacter, Spongiobacter, Vibrio, and Alteromonas, which were isolated on media with either DMSP or DMS as the sole carbon source, comprised the majority of clones retrieved from coral mucus and tissue 16S rRNA gene clone libraries. Clones affiliated with Roseobacter sp. constituted 28% of the M. aequituberculata tissue libraries, while 59% of the clones from the A. millepora libraries were affiliated with sequences related to the Spongiobacter genus. Vibrio spp. were commonly isolated from DMS and acrylic acid enrichments and were also present in 16S rRNA gene libraries from coral mucus, suggesting that under "normal" environmental conditions, they are a natural component of coral-associated communities. Genes homologous to dddD, and dddL, previously implicated in DMSP degradation, were also characterized from isolated strains, confirming that bacteria associated with corals have the potential to metabolize this sulfur compound when present in coral tissues. Our results demonstrate that DMSP, DMS, and acrylic acid potentially act as nutrient sources for coral-associated bacteria and that these sulfur compounds are likely to play a role in structuring bacterial communities in corals, with important consequences for the health of both corals and coral reef ecosystems.Dimethylsulfoniopropionate (DMSP) is an organic sulfur compound implicated in the formation of clouds via its cleavage product dimethyl sulfide (DMS) and therefore has the potential to exert major cooling effects on climate (9, 38). The production of DMSP is mainly restricted to a few classes of marine macro-and microalgae (27,68), with the main producers being phytoplankton species belonging to prymnesiophyte and dinoflagellate taxa (28,62,67). Recently, significant concentrations of DMSP and DMS have been recorded in association with animals that harbor symbiotic algae such as scleractinian corals and giant clams (7,8,68), raising questions about the role of coral reefs in sulfur cycling. The densities of symbiotic dinoflagellates (genus Symbiodinium, commonly known as zooxanthellae) in coral tissues are similar to those recorded for dinoflagellates in phytoplankton blooms (11, 68). Since dinoflagellates are among the most significant producers of DMSP and high intracellular concentrations of DMSP have been found in both cultured zooxanthellae (26) and scleractinian corals (6-8, 25), these observations suggest that endos...

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Section: Discussionsupporting

confidence: 58%

Section: Discussionsupporting

confidence: 54%

See 1 more Smart Citation

Coral-Associated Bacteria and Their Role in the Biogeochemical Cycling of Sulfur

Raina

Tapiolas

Willis

et al. 2009

Appl Environ Microbiol

380

320

View full text Add to dashboard Cite

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“…The majority of DMSP (50 to 90%) is demethylated to 3-methiolpropionate (MMPA), ultimately producing sulfur and carbon intermediates which are incorporated into microbial biomass or further oxidized (29,44). A competing metabolic pathway results in the production of dimethylsulfide (DMS) from DMSP (16,21). DMS represents a major source of biogenic sulfur to the atmosphere, where oxidation products form cloud condensation nuclei and ultimately influence radiative backscatter (2,33,49).…”

mentioning

confidence: 99%

Bacterial Dimethylsulfoniopropionate Degradation Genes in the Oligotrophic North Pacific Subtropical Gyre

Varaljay

Gifford

Wilson

et al. 2012

Appl Environ Microbiol

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ABSTRACTDimethylsulfoniopropionate (DMSP) is an organic sulfur compound that is rapidly metabolized by marine bacteria either by cleavage to dimethylsulfide (DMS) or demethylation to 3-methiolpropionate. The abundance and diversity of genes encoding bacterial DMS production (dddP) and demethylation (dmdA) were measured in the North Pacific subtropical gyre (NPSG) between May 2008 and February 2009 at Station ALOHA (22°45′N, 158°00′W) at two depths: 25 m and the deep chlorophyll maximum (DCM; ∼100 m). The highest abundance ofdmdAgenes was in May 2008 at 25 m, with ∼16.5% of cells harboring a gene in one of the eight subclades surveyed, while the highest abundance ofdddPgenes was in July 2008 at 25 m, with ∼2% of cells harboring a gene. ThedmdAgene pool was consistently dominated by homologs from SAR11 subclades, which was supported by findings in metagenomic data sets derived from Station ALOHA. Expression of the SAR11dmdAgenes was low, with typical transcript:gene ratios between 1:350 and 1:1,400. The abundance of DMSP genes was statistically different between 25 m and the DCM and correlated with a number of environmental variables, including primary production, photosynthetically active radiation, particulate DMSP, and DMS concentrations. At 25 m,dddPabundance was positively correlated with pigments that are diagnostic of diatoms; at the DCM,dmdAabundance was positively correlated with temperature. Based on gene abundance, we hypothesize that SAR11 bacterioplankton dominate DMSP cycling in the oligotrophic NPSG, with lesser but consistent involvement of other members of the bacterioplankton community.

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“…When released from such organisms, other marine microbes can use several wholly different ways to catabolize DMSP (Yoch, 2002;Johnston et al, 2007;Howard et al, 2008). Worldwide, these biotransformations annually turn over B10 9 tons of DMSP.…”

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confidence: 99%

The opportunistic coral pathogen Aspergillus sydowii contains dddP and makes dimethyl sulfide from dimethylsulfoniopropionate

et al. 2009

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The ascomycete Aspergillus sydowii is associated with a serious epizootic of sea fan corals in the Caribbean. Corals are rich in the compatible solute, dimethylsulfoniopropionate (DMSP), produced by their symbionts, the dinoflagellate Symbiodinium. As other Aspergillus species can catabolize DMSP, liberating dimethyl sulfide (DMS) in the process, we tested A. sydowii strains, obtained from diseased corals and other environments, for this Ddd þ phenotype. All the strains, irrespective of their geographical or environmental origins, made DMS from DMSP, and all of them contained homologs (487% identical) of the dddP gene, which encodes an enzyme that releases DMS from DMSP and which occurs in other Ddd þ fungi and in some marine bacteria. The dddP gene was likely acquired by the Aspergillus fungi by inter-domain horizontal gene transfer from a-proteobacteria.

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Molecular diversity of bacterial production of the climate-changing gas, dimethyl sulphide, a molecule that impinges on local and global symbioses

Cited by 37 publications

References 50 publications

Coral-Associated Bacteria and Their Role in the Biogeochemical Cycling of Sulfur

Coral-Associated Bacteria and Their Role in the Biogeochemical Cycling of Sulfur

Bacterial Dimethylsulfoniopropionate Degradation Genes in the Oligotrophic North Pacific Subtropical Gyre

The opportunistic coral pathogen Aspergillus sydowii contains dddP and makes dimethyl sulfide from dimethylsulfoniopropionate

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