Cellular traits regulate fluorescence-based light-response phenotypes of coral photosymbionts living in-hospite.

Diversity across algal family Symbiodiniaceae contributes to the environmental resilience of certain coral species. Chlorophyll-a fluorescence measurements are frequently used to determine symbiont health and resilience, but more work is needed to refine these tools and establish how they relate to underlying cellular traits. We examined trait diversity in symbionts from the generas Cladocopium and Durusdinium, collected from 12 aquacultured coral species. Photophysiological metrics (ΦPSII, σPSII, ρ, τ1, τ2, antenna bed quenching, non-photochemical quenching, and qP) were assessed using a prototype multi-spectral fluorometer over a variable light protocol which yielded a total of 1,360 individual metrics. Photophysiological metrics were then used to establish four unique light-response phenotypic variants. Corals harboring C15 were predominantly found within a single light-response phenotype which clustered separately from all other coral fragments. The majority of Durusdinium dominated colonies also formed a separate light-response phenotype which it shared with a few C1 dominated corals. C15 and D1 symbionts appear to differ in which mechanisms they use to dissipate excess light energy. Spectrally dependent variability is also observed across light-response phenotypes that may relate to differences in photopigment utilization. Symbiont cell biochemical and structural traits (atomic C:N:P, cell size, chlorophyll-a, neutral lipid content) was also assessed within each sample and differ across light-response phenotypes, linking photophysiological metrics with underlying primary cellular traits. Strong correlations between first- and second-order traits, such as Quantum Yield and cellular N:P content, or light dissipation pathways (qP and NPQ) and C:P underline differences across symbiont types and may also provide a means for using fluorescence-based metrics as biomarkers for certain primary-cellular traits.

Coral physiology and microbiome dynamics under combined warming and ocean acidification.

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.

Microelectrode characterization of coral daytime interior pH and carbonate chemistry.

Reliably predicting how coral calcification may respond to ocean acidification and warming depends on our understanding of coral calcification mechanisms. However, the concentration and speciation of dissolved inorganic carbon (DIC) inside corals remain unclear, as only pH has been measured while a necessary second parameter to constrain carbonate chemistry has been missing. Here we report the first carbonate ion concentration ([CO3(2-)]) measurements together with pH inside corals during the light period. We observe sharp increases in [CO3(2-)] and pH from the gastric cavity to the calcifying fluid, confirming the existence of a proton (H(+)) pumping mechanism. We also show that corals can achieve a high aragonite saturation state (Ωarag) in the calcifying fluid by elevating pH while at the same time keeping [DIC] low. Such a mechanism may require less H(+)-pumping and energy for upregulating pH compared with the high [DIC] scenario and thus may allow corals to be more resistant to climate change related stressors.

Physiological response to elevated temperature and pCO2 varies across four Pacific coral species: Understanding the unique host+symbiont response.

The physiological response to individual and combined stressors of elevated temperature and pCO2 were measured over a 24-day period in four Pacific corals and their respective symbionts (Acropora millepora/Symbiodinium C21a, Pocillopora damicornis/Symbiodinium C1c-d-t, Montipora monasteriata/Symbiodinium C15, and Turbinaria reniformis/Symbiodinium trenchii). Multivariate analyses indicated that elevated temperature played a greater role in altering physiological response, with the greatest degree of change occurring within M. monasteriata and T. reniformis. Algal cellular volume, protein, and lipid content all increased for M. monasteriata. Likewise, S. trenchii volume and protein content in T. reniformis also increased with temperature. Despite decreases in maximal photochemical efficiency, few changes in biochemical composition (i.e. lipids, proteins, and carbohydrates) or cellular volume occurred at high temperature in the two thermally sensitive symbionts C21a and C1c-d-t. Intracellular carbonic anhydrase transcript abundance increased with temperature in A. millepora but not in P. damicornis, possibly reflecting differences in host mitigated carbon supply during thermal stress. Importantly, our results show that the host and symbiont response to climate change differs considerably across species and that greater physiological plasticity in response to elevated temperature may be an important strategy distinguishing thermally tolerant vs. thermally sensitive species.

Coral energy reserves and calcification in a high-CO2 world at two temperatures.

Rising atmospheric CO2 concentrations threaten coral reefs globally by causing ocean acidification (OA) and warming. Yet, the combined effects of elevated pCO2 and temperature on coral physiology and resilience remain poorly understood. While coral calcification and energy reserves are important health indicators, no studies to date have measured energy reserve pools (i.e., lipid, protein, and carbohydrate) together with calcification under OA conditions under different temperature scenarios. Four coral species, Acropora millepora, Montipora monasteriata, Pocillopora damicornis, Turbinaria reniformis, were reared under a total of six conditions for 3.5 weeks, representing three pCO2 levels (382, 607, 741 µatm), and two temperature regimes (26.5, 29.0 °C) within each pCO2 level. After one month under experimental conditions, only A. millepora decreased calcification (-53%) in response to seawater pCO2 expected by the end of this century, whereas the other three species maintained calcification rates even when both pCO2 and temperature were elevated. Coral energy reserves showed mixed responses to elevated pCO2 and temperature, and were either unaffected or displayed nonlinear responses with both the lowest and highest concentrations often observed at the mid-pCO2 level of 607 µatm. Biweekly feeding may have helped corals maintain calcification rates and energy reserves under these conditions. Temperature often modulated the response of many aspects of coral physiology to OA, and both mitigated and worsened pCO2 effects. This demonstrates for the first time that coral energy reserves are generally not metabolized to sustain calcification under OA, which has important implications for coral health and bleaching resilience in a high-CO2 world. Overall, these findings suggest that some corals could be more resistant to simultaneously warming and acidifying oceans than previously expected.