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 coral-associated 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.

FIG. 1.

Composition of the coral clone libraries. (a) M. aequituberculata tissues (181 clones); (b) A. millepora tissues (172 clones); (c) M. aequituberculata mucus (91 clones); (d) A. millepora mucus (91 clones); (e) seawater libraries (91 clones). The large pie charts represent the contents of the libraries at the class level. The smaller pies represent the percentage proportions of the different isolates (at the genus level). Replicate tissue libraries were highly similar, and therefore clone sequence data were pooled for these samples.

FIG. 2.

Correspondence analysis plot showing the relationships between clone libraries from mucus, tissue and skeletal samples of the corals, A. millepora and M. aequituberculata, and the main sulfur-degrading bacterial genera isolated in the present study. AM, A. millepora (tissue or mucus libraries); MA, M. aequituberculata (tissue or mucus libraries). Total inertia = 1.5586, chi² = 427.37, df = 42, P = 0.000.

FIG. 3.

¹H NMR spectra of acrylic acid enrichment (50 μM) in MASW medium with Vibrio fortis (a) or Vibrio harveyi (b), both isolated from A. millepora tissues, and control (c) at 7 days after the acrylic acid inoculation. The three peaks of the acrylic acid signal (position 1) are only visible in the control; the other peaks represent the solvent (water) (position 2) and methanol (position 3).