Volatile organic compounds (VOCs) are constituents of marine ecosystems including coral reefs, where they are sources of atmospheric reactivity, indicators of ecosystem state, components of defense strategies, and infochemicals. Most VOCs result from sunlight-related processes; however, their light-driven dynamics are still poorly understood. We studied the spatial variability of a suite of VOCs, including dimethylsulfide (DMS), and the other dimethylsulfoniopropionate-derived compounds (DMSPCs), namely, DMSP, acrylate, and dimethylsulfoxide (DMSO), in waters around colonies of two scleractinian corals ( Acropora pulchra and Pocillopora sp.) and the brown seaweed Turbinaria ornata in Mo’orean reefs, French Polynesia. Concentration gradients indicated that the corals were sources of DMSPCs, but less or null sources of VOCs other than DMS, while the seaweed was a source of DMSPCs, carbonyl sulfide (COS), and poly-halomethanes. A focused study was conducted around an A. pulchra colony where VOC and DMSPC concentrations and free-living microorganism abundances were monitored every 6 h over 30 h. DMSPC concentrations near the polyps paralleled sunlight intensity, with large diurnal increases and nocturnal decrease. rDNA metabarcoding and metagenomics allowed the determination of microbial diversity and the relative abundance of target functional genes. Seawater near coral polyps was enriched in DMS as the only VOC, plus DMSP, acrylate, and DMSO, with a large increase during the day, coinciding with high abundances of symbiodiniacean sequences. Only 10 cm below, near the coral skeleton colonized by a turf alga, DMSPC concentrations were much lower and the microbial community was significantly different. Two meters down current from the coral, DMSPCs decreased further and the microbial community was more similar to that near the polyps than that near the turf alga. Several DMSP cycling genes were enriched in near-polyp with respect to down-current waters, namely, the eukaryotic DMS production and DMS oxidation encoding genes, attributed to the coral and the algal symbiont, and the prokaryotic DMS production gene dddD , harbored by coral-associated Gammaproteobacteria . Our results suggest that solar radiation-induced oxidative stress caused the release of DMSPCs by the coral holobiont, either directly or through symbiont expulsion. Strong chemical and biological gradients occurred in the water between the coral branches, which we attribute to layered hydrodynamics.
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Concentrations, sources, and biological consumption of acrylate and DMSP in the tropical Pacific and coral reef ecosystem in Mo’orea, French Polynesia
Shallow-water coral reefs hold large quantities of acrylate and its precursor dimethylsulfoniopropionate (DMSP), but production and removal processes for these compounds are poorly characterized. Here we determined the concentrations and cycling of acrylate and DMSP in a transect from a coral reef ecosystem to the open ocean, 2 km beyond the reef in Mo’orea, French Polynesia, during April 2018. Concentrations of dissolved acrylate and DMSP were low throughout the reef-ocean transect, ranging from 0.8–3.9 nM and 0.2–3.0 nM, respectively, with no difference observed between the coral reef and open ocean when comparing mean concentrations (± std dev) of dissolved acrylate (1.7 ± 0.7 vs 2.3 ± 0.8 nM) or DMSP (0.9 ± 0.7 vs 1.3 ± 0.6 nM). In the coral reef, dissolved acrylate was rapidly taken up by the heterotrophic community with a fast turnover time averaging ~ 6 h, six times faster than in the open ocean, and nearly as fast as the average turnover time of dissolved DMSP (~ 3 h). A clear diel trend was observed for the heterotrophic consumption of dissolved acrylate and DMSP in the coral reef, with higher uptake rate constants during daylight hours, synchronized with the larger daytime release of acrylate and DMSP from the coral compared to the nighttime release of these compounds. We also measured photochemical production rates of acrylate in Mo’orean waters, but rates were one to two orders of magnitude slower compared to its rates of biological consumption. Coral and macroalgae were the main sources of dissolved acrylate and DMSP to the reef ecosystem. Our results indicate there is rapid turnover of acrylate and DMSP in the coral reef with a tight coupling between production and removal pathways that maintain dissolved concentrations of these two compounds at very low levels. These algal and coral-derived substrates serve as important chemical links between the coral and heterotrophic communities, two fundamental components in the ecological network in coral reefs.
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- Award ID(s):
- 1756907
- NSF-PAR ID:
- 10396691
- Date Published:
- Journal Name:
- Frontiers in Marine Science
- Volume:
- 9
- ISSN:
- 2296-7745
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fmars.2022.911522
