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Biogenic volatile organic compounds (VOCs) play key roles in coral reef ecosystems, where, together with dimethylated sulfur compounds, they are indicators of ecosystem health and are used as defense strategies and infochemicals. Assessment and prediction of the exchange rates of VOCs between the oceans and atmosphere, with implications for atmospheric reactivity and climate, are hampered by poor knowledge of the regulating processes and their temporal variability, including diel cycles. Here, we measured the variation over 36h of the concentrations of DMSPCs (dimethylsulfoniopropionate (DMSP)-related compounds, namely DMSP, dimethylsulfoxide, acrylate, dimethylsulfide, and methanethiol as dimethyl disulfide) and VOCs (COS, CS2, isoprene, the iodomethanes CH3I and CH2ClI, and the bromomethanes CHBr3and CH2Br2), in surface waters inside the shallow, northern coral-reef lagoon of Mo’orea (French Polynesia) and 4 km offshore, in the tropical open ocean. Comparisons with concurrent measurements of sea surface temperature, solar radiation, biogeochemical variables (nutrients, organic matter), and the abundances and taxonomic affiliations of microbial plankton were conducted with the aim to explain interconnections between DMSPCs, VOCs, and their environment across diel cycles. In open ocean waters, deeper surface mixing and low nutrient levels resulted in low phytoplankton biomass and bacterial activity. Consequently, the diel patterns of VOCs were more dependent on photochemical reactions, with daytime increases for several compounds including dissolved dimethylsulfoxide, COS, CS2, CH3I, and CH2ClI. A eukaryotic phytoplankton assemblage dominated by dinoflagellates and haptophytes provided higher cell-associated DMSP concentrations, yet the occurrence of DMSP degradation products (dimethylsulfide, dimethyl disulfide) was limited by photochemical loss. Conversely, in the shallow back reef lagoon the proximity of seafloor sediments, corals and abundant seaweeds resulted in higher nutrient levels, more freshly-produced organic matter, higher bacterial activity, and larger algal populations ofMamiellales, diatoms andCryptomonadales. Consequently, DMSP and dimethylsulfoxide concentrations were lower but those of most VOCs were higher. A combination of photobiological and photochemical processes yielded sunny-daytime increases and nighttime decreases of dimethylsulfide, dimethyl disulfide, COS, isoprene, iodomethanes and bromomethanes. Our results illustrate the important role of solar radiation in DMSPC and VOC cycling, and are relevant for the design of sampling strategies that seek representative and comparable measurements of these compounds.
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Spatial and diel patterns of volatile organic compounds, DMSP-derived compounds, and planktonic microorganisms around a tropical scleractinian coral colony
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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- Award ID(s):
- 1756907
- PAR ID:
- 10396842
- 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.2022.944141
