Spatial and diel patterns of volatile organic compounds, DMSP-derived compounds, and planktonic microorganisms around a tropical scleractinian coral colony

Abstract

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.

Concentrations, sources, and biological consumption of acrylate and DMSP in the tropical Pacific and coral reef ecosystem in Mo’orea, French Polynesia

“…A large percentage of acrylate, ranging from 50 to 95%, was present in the dissolved phase in all surface waters, consistent with previous culture studies (Tyssebotn, 2015;. Dissolved and particulate acrylate and DMSP concentrations reported in this section only include water samples more than a meter away from coral and do not include concentrations in the coral holobiont or in close proximity to the coral; concentrations in these environments are expected to be substantially higher as discussed below (also see Tapiolas et al, 2010;Raina et al, 2013;Tapiolas et al, 2013;Masdeu-Navarro et al, 2022).…”

“…In all our samples, greater than 90% of the DMSO was detected in the dissolved phase (Figure 2C), with very little DMSO present in the particulate pool due to its rapid diffusion out of the cell into the dissolved phase (Spiese et al, 2016). Compared to DMSP d and DMS (DMS results presented in Masdeu-Navarro et al, 2022), DMSO d was the main contributor to the dissolved organic sulfur pool averaging nearly 3 nM throughout Mo'orea study. There are several potential sources of DMSO d in our study area including inputs from the particulate phase (e.g., from DMSO production in planktonic algae, macroalgae, the coral holobiont and subsequent diffusion into the dissolved phase), photochemical oxidation of DMS, or bacterial production from DMS (e.g., trimethylamine monooxygenase activity; Lidbury et al, 2016).…”

“…Two photos depicting typical intermittent reef patches surrounded by sandy bottom present in the Mo'orea coral reef lagoonal system at station BR and the Temae coral reef are shown in Figure S1. A google map showing an aerial overview of the island of Mo'orea and the study area is presented in our companion paper, along with photos showing our protocol used to collect samples close to the coral colonies (Masdeu-Navarro et al, 2022).…”

“…Thus, this common coral may be a smaller source of dissolved acrylate and DMSP to the Mo'orea coral reef system compared to A. pulchra (also see Figure 4). Overall, A. pluchara was a strong source of dissolved acrylate, DMS (DMS data in Masdeu-Navarro et al, 2022), DMSP and DMSO, whereas Pocillopora sp. was a weak source for dissolved acrylate and DMSP and not a source of DMSO or DMS (Masdeu-Navarro et al, 2022).…”

“…Corals can expel ~10% of their algal symbionts on a daily basis and even more when they are physically or chemically stressed (Broadbent and Jones, 2006), with the expelled Symbiodiniaceae exposed to stress and mortality similar to planktonic phytoplankton. This may result in releases of large quantities of DMSP and acrylate (Masdeu-Navarro et al, 2022) that will feed the fast microbial cycling of dissolved carbon and sulfur in the coral reef.…”