Coral physiology and microbiome dynamics under combined warming and ocean acidification

Abstract

Rising seawater temperature and ocean acidification threaten the survival of coral reefs. The relationship between coral physiology and its microbiome may reveal why some corals are more resilient to these global change conditions. Here, we conducted the first experiment to simultaneously investigate changes in the coral microbiome and coral physiology in response to the dual stress of elevated seawater temperature and ocean acidification expected by the end of this century. Two species of corals, Acropora millepora containing the thermally sensitive endosymbiont C21a and Turbinaria reniformis containing the thermally tolerant endosymbiont Symbiodinium trenchi, were exposed to control (26.5°C and pCO2 of 364 μatm) and treatment (29.0°C and pCO2 of 750 μatm) conditions for 24 days, after which we measured the microbial community composition. These microbial findings were interpreted within the context of previously published physiological measurements from the exact same corals in this study (calcification, organic carbon flux, ratio of photosynthesis to respiration, photosystem II maximal efficiency, total lipids, soluble animal protein, soluble animal carbohydrates, soluble algal protein, soluble algal carbohydrate, biomass, endosymbiotic algal density, and chlorophyll a). Overall, dually stressed A. millepora had reduced microbial diversity, experienced large changes in microbial community composition, and experienced dramatic physiological declines in calcification, photosystem II maximal efficiency, and algal carbohydrates. In contrast, the dually stressed coral T. reniformis experienced a stable and more diverse microbiome community with minimal physiological decline, coupled with very high total energy reserves and particulate organic carbon release rates. Thus, the microbiome changed and microbial diversity decreased in the physiologically sensitive coral with the thermally sensitive endosymbiotic algae but not in the physiologically tolerant coral with the thermally tolerant endosymbiont. Our results confirm recent findings that temperature-stress tolerant corals have a more stable microbiome, and demonstrate for the first time that this is also the case under the dual stresses of ocean warming and acidification. We propose that coral with a stable microbiome are also more physiologically resilient and thus more likely to persist in the future, and shape the coral species diversity of future reef ecosystems.

Disentangling the complex microbial community of coral reefs using standardized Autonomous Reef Monitoring Structures (ARMS)

“…Importantly, SST was identified as a key driver for various bacterial families in the reef community, in line with its critical role for the microbial communities comprising the coral microbiome (Grottoli et al, ), and as reported in global microbial plankton studies (Sunagawa et al, ). Various bacterial families showed correlations with temperature (e.g., Planctomycetaceae, SAR116 and Phyllobacteriaceae having a positive relationship, and Flammeovirgaceae having a negative correlation).…”

Thresholds and drivers of coral calcification responses to climate change

“…However, our large residual heterogeneities (Table ) suggest additional contributing factors. Important physiological aspects such as adaptation and acclimatization (Hume et al., ; Palumbi et al., ; Pandolfi, ), species interactions (Evensen & Edmunds, ; Kordas, Harley, & O'Connor, ), photosynthesis (Langdon & Atkinson, ), coral microbiome stability (Grottoli et al., ), and compounding stressors (Carpenter et al., ; Comeau, Carpenter, & Edmunds, ) can have profound impacts on coral resistance to climate change and were insufficiently represented in our analysis. While the differences in vulnerabilities and environmental circumstances illustrated above can aid coral reef management identifying local refuges and conservation priorities, the main finding of this study illustrates the urgent need for a global effort to reduce carbon emissions or we risk losing major ecosystem services via loss of the ability of corals to build reefs.…”

Coral microbiome diversity reflects mass coral bleaching susceptibility during the 2016 El Niño heat wave

“…Microbiomes play a key role in contributing to coral fitness over space and time (Putnam et al, ; Suggett et al, ) and are known to exhibit broad changes across reefs persisting under different environmental conditions (Roder et al, ) and when subjected to atypical stress (Grottoli et al, ; Röthig et al, ; Ziegler, Seneca et al, ). Here, we provide the first characterization of the microbial community composition (i.e., Symbiodiniaceae and bacteria) for key reef‐building coral taxa of Seychelles across two different environments.…”