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

Abstract

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...

Coral reef invertebrate microbiomes correlate with the presence of photosymbionts

“…Recent studies, however, indicate that other members of the coral holobiont (in particular Symbiodinium dinoflagellates) also influence microbial community structure through release of complex carbon-containing exudates including dimethylsulfoniopropionate (DMSP; Ikeda and Miyachi, 1995;Raina et al, 2009Raina et al, , 2010. DMSP can be degraded to dimethylysulphide, a central molecule in the global sulphur cycle, which diffuses from the ocean into the atmosphere where it influences cloud formation, with consequences for atmospheric chemistry, local climate and water temperature (Ayers and Gras, 1991;Andreae and Crutzen, 1997).…”

“…These OTUs are all affiliated with species implicated in the metabolism of complex organic molecules such as DMSP and dimethylysulphide. For example, previous studies have identified abundant bacteria within the Oceanospirillales that are able to metabolise DMSP in the coral Acropora millepora (Raina et al, 2009 Figure 1 Redundancy analysis (RDA) summarising variation in the composition of marine invertebrate-associated microbial communities that was attributable to the presence-absence of photosymbionts. The filled shapes represent individual samples collected from each invertebrate species.…”

A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals

“…Two different basal media were used to determine the DMSP metabolic capabilities of V. coralliilyticus: a modified marine ammonium salt medium (Raina et al, 2009) lacking any carbon source, and a modified basal salt medium lacking any sulfur source (Fuse et al, 2000). DMSP was added to both the media (1 mM final concentration) and acted either as a sole carbon source or as a sole sulfur source.…”

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

“…DddD homologs occur not only in marine a-and gproteobacteria that were already known to have Ddd þ phenotypes, but also in the terrestrial bacteria, Burkholderia ambifaria and Rhizobium NGR234, both of which, perhaps significantly, interact with higher plants . Raina et al (2009) recently isolated g-and a-proteobacteria that grew on DMSP as sole carbon source from the mucus or skeletons of the coral Montipora, which interacts with DMSP-containing zooxanthellae (Hill et al, 1995). Having shown here that at least some fungi that associate with corals have a Ddd þ phenotype, it will be of interest to know the relative contributions of bacteria and Column (1) shows A. sydowii strains as in Rypien et al (2008).…”