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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 CHBr3 and 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 of Mamiellales, diatoms and Cryptomonadales. 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.

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.

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.

Reef-building corals are among the largest producers of dimethylsulfoniopropionate (DMSP), an essential compound in marine biogeochemical cycles. DMSP can be catabolised in coral mucus by a wide diversity of coral-associated bacteria, where it can either be demethylated, leading to the incorporation of sulfur and carbon into bacterial biomass – or cleaved by lyases, releasing the climatically-active gas dimethyl sulfide (DMS). It has been demonstrated that thermal stress increases DMSP concentrations in many coral species, however the effect of increased DMSP availability on coral-associated bacteria has not been explored. Here we performed thermal stress experiments to examine how changes in DMSP availability impact bacterial degradation pathways in the mucus of Acropora millepora. DMSP concentrations increased with temperature, reaching a maximum of 177.3 μM after 10 days of heat stress, which represents the highest concentration of DMSP recorded in any environment to date. Bacterial communities in coral mucus were significantly different from the surrounding seawater, yet they did not vary significantly between temperature or time. However, during thermal stress, when DMSP concentrations increased, a significant increase in the abundance of both the demethylation gene dmdA and the cleavage gene dddP were recorded. Importantly, our results show that for the highest DMSP concentrations recorded (above 30 μM), the cleavage pathway became more abundant than the demethylation pathway. This suggests that under high DMSP concentrations characteristic of heat stress, a larger fraction of the DMSP pool in the coral mucus is likely catabolised through the DMS-producing cleavage pathway.

Abstract Repeat marine heat wave‐induced mass coral bleaching has decimated reefs in Seychelles for 35 years, but how coral‐associated microbial diversity (microalgal endosymbionts of the family Symbiodiniaceae and bacterial communities) potentially underpins broad‐scale bleaching dynamics remains unknown. We assessed microbiome composition during the 2016 heat wave peak at two contrasting reef sites (clear vs. turbid) in Seychelles, for key coral species considered bleaching sensitive (Acropora muricata, Acropora gemmifera) or tolerant (Porites lutea, Coelastrea aspera). For all species and sites, we sampled bleached versus unbleached colonies to examine how microbiomes align with heat stress susceptibility. Over 30% of all corals bleached in 2016, half of which were from Acropora sp. and Pocillopora sp. mass bleaching that largely transitioned to mortality by 2017. Symbiodiniaceae ITS2‐sequencing revealed that the two Acropora sp. and P. lutea generally associated with C3z/C3 and C15 types, respectively, whereas C. aspera exhibited a plastic association with multiple D types and two C3z types. 16S rRNA gene sequencing revealed that bacterial communities were coral host‐specific, largely through differences in the most abundant families, Hahellaceae (comprising Endozoicomonas), Rhodospirillaceae, and Rhodobacteraceae. Both Acropora sp. exhibited lower bacterial diversity, species richness, and community evenness compared to more bleaching‐resistant P. lutea and C. aspera. Different bleaching susceptibility among coral species was thus consistent with distinct microbiome community profiles. These profiles were conserved across bleached and unbleached colonies of all coral species. As this pattern could also reflect a parallel response of the microbiome to environmental changes, the detailed functional associations will need to be determined in future studies. Further understanding such microbiome‐environmental interactions is likely critical to target more effective management within oceanically isolated reefs of Seychelles.

Abstract Background Climate change causes the breakdown of the symbiotic relationships between reef-building corals and their photosynthetic symbionts (genus Symbiodinium), with thermal anomalies in 2015–2016 triggering the most widespread mass coral bleaching on record and unprecedented mortality on the Great Barrier Reef. Targeted studies using specific coral stress indicators have highlighted the complexity of the physiological processes occurring during thermal stress, but have been unable to provide a clear mechanistic understanding of coral bleaching. Results Here, we present an extensive multi-trait-based study in which we compare the thermal stress responses of two phylogenetically distinct and widely distributed coral species, Acropora millepora and Stylophora pistillata, integrating 14 individual stress indicators over time across a simulated thermal anomaly. We found that key stress responses were conserved across both taxa, with the loss of symbionts and the activation of antioxidant mechanisms occurring well before collapse of the physiological parameters, including gross oxygen production and chlorophyll a. Our study also revealed species-specific traits, including differences in the timing of antioxidant regulation, as well as drastic differences in the production of the sulfur compound dimethylsulfoniopropionate during bleaching. Indeed, the concentration of this antioxidant increased two-fold in A. millepora after the corals started to bleach, while it decreased 70% in S. pistillata. Conclusions We identify a well-defined cascading response to thermal stress, demarking clear pathophysiological reactions conserved across the two species, which might be central to fully understanding the mechanisms triggering thermally induced coral bleaching. These results highlight that bleaching is a conserved mechanism, but specific adaptations linked to the coral’s antioxidant capacity drive differences in the sensitivity and thus tolerance of each coral species to thermal stress.

Abstract Coral reefs are deteriorating under climate change as oceans continue to warm and acidify and thermal anomalies grow in frequency and intensity. In vitro experiments are widely used to forecast reef-building coral health into the future, but often fail to account for the complex ecological and biogeochemical interactions that govern reefs. Consequently, observations from coral communities under naturally occurring extremes have become central for improved predictions of future reef form and function. Here, we present a semi-enclosed lagoon system in New Caledonia characterised by diel fluctuations of hot-deoxygenated water coupled with tidally driven persistently low pH, relative to neighbouring reefs. Coral communities within the lagoon system exhibited high richness (number of species = 20) and cover (24–35% across lagoon sites). Calcification rates for key species (Acropora formosa, Acropora pulchra, Coelastrea aspera and Porites lutea) for populations from the lagoon were equivalent to, or reduced by ca. 30–40% compared to those from the reef. Enhanced coral respiration, alongside high particulate organic content of the lagoon sediment, suggests acclimatisation to this trio of temperature, oxygen and pH changes through heterotrophic plasticity. This semi-enclosed lagoon therefore provides a novel system to understand coral acclimatisation to complex climatic scenarios and may serve as a reservoir of coral populations already resistant to extreme environmental conditions.

Light availability is considered a key factor regulating the thermal sensitivity of reef building corals, where excessive excitation of photosystem II (PSII) further exacerbates pressure on photochemical pathways already compromised by heat stress. Coral symbionts acclimate to changes in light availability (photoacclimation) by continually fine-tuning the photochemical operating efficiency of PSII. However, how this process adjusts throughout the warmest months in naturally heat-tolerant or sensitive species is unknown, and whether this influences the capacity to tolerate transient heat stress is untested. We therefore examined the PSII photophysiology of 10 coral species (with known thermal tolerances) from shallow reef environments at Heron Island (Great Barrier Reef, Australia), in spring (October-November, 2015) vs. summer (February-March, 2016). Corals were maintained in flow-through aquaria and rapid light curve (RLC) protocols using pulse amplitude modulated (PAM) fluorometry captured changes in the PSII photoacclimation strategy, characterized as the minimum saturating irradiance (Ek), and the extent of photochemical ([1 – C], operating efficiency) vs. non-photochemical ([1 – Q]) energy dissipation. Values of Ek across species were >2-fold higher in all coral species in spring, consistent with a climate of higher overall light exposure (i.e., higher PAR from lower cloud cover, rainfall and wind speed) compared with summer. Summer decreases in Ek were combined with a shift toward preferential photochemical quenching in all species. All coral species were subsequently subjected to thermal stress assays. An equivalent temperature-ramping profile of 1°C increase per day and then maintenance at 32°C was applied in each season. Despite the significant seasonal photoacclimation, the species hierarchy of thermal tolerance [maximum quantum yields of PSII (Fv/Fm), monitored at dawn and dusk] did not shift between seasons, except for Pocillopora damicornis (faster declines in summer) and Stylophora pistillata (total mortality in spring). Furthermore, the strategy for dealing with light energy (i.e., preferential photochemical vs. non-photochemical quenching) was unchanged for thermally tolerant species across seasons, whereas thermally sensitive species switched between preferential [1 – Q] and [1 – C] from spring to summer. We discuss how such traits can potentially be used as a diagnostic of thermal tolerance under non-stressed conditions.