Impact of Ocean Warming and Acidification on Symbiosis Establishment and Gene Expression Profiles in Recruits of Reef Coral Acropora intermedia.
ABSTRACT: The onset of symbiosis and the early development of most broadcast spawning corals play pivotal roles in recruitment success, yet these critical early stages are threatened by multiple stressors. However, molecular mechanisms governing these critical processes under ocean warming and acidification are still poorly understood. The present study investigated the interactive impact of elevated temperature (?28.0°C and ?30.5°C) and partial pressure of carbon dioxide (pCO2) (?600 and ?1,200 ?atm) on early development and the gene expression patterns in juvenile Acropora intermedia over 33 days. The results showed that coral survival was >89% and was unaffected by high temperature, pCO2, or the combined treatment. Notably, high temperature completely arrested successful symbiosis establishment and the budding process, whereas acidification had a negligible effect. Moreover, there was a positive exponential relationship between symbiosis establishment and budding rates (y = 0.0004e6.43x, R = 0.72, P < 0.0001), which indicated the importance of symbiosis in fueling asexual budding. Compared with corals at the control temperature (28°C), those under elevated temperature preferentially harbored Durusdinium spp., despite unsuccessful symbiosis establishment. In addition, compared to the control, 351 and 153 differentially expressed genes were detected in the symbiont and coral host in response to experimental conditions, respectively. In coral host, some genes involved in nutrient transportation and tissue fluorescence were affected by high temperature. In the symbionts, a suite of genes related to cell growth, ribosomal proteins, photosynthesis, and energy production was downregulated under high temperatures, which may have severely hampered successful cell proliferation of the endosymbionts and explains the failure of symbiosis establishment. Therefore, our results suggest that the responses of symbionts to future ocean conditions could play a vital role in shaping successful symbiosis in juvenile coral.
Project description:Diurnal pCO2 fluctuations have the potential to modulate the biological impact of ocean acidification (OA) on reef calcifiers, yet little is known about the physiological and biochemical responses of scleractinian corals to fluctuating carbonate chemistry under OA. Here, we exposed newly settled Pocillopora damicornis for 7 days to ambient pCO2, steady and elevated pCO2 (stable OA) and diurnally fluctuating pCO2 under future OA scenario (fluctuating OA). We measured the photo-physiology, growth (lateral growth, budding and calcification), oxidative stress and activities of carbonic anhydrase (CA), Ca-ATPase and Mg-ATPase. Results showed that while OA enhanced the photochemical performance of in hospite symbionts, it also increased catalase activity and lipid peroxidation. Furthermore, both OA treatments altered the activities of host and symbiont CA, suggesting functional changes in the uptake of dissolved inorganic carbon (DIC) for photosynthesis and calcification. Most importantly, only the fluctuating OA treatment resulted in a slight drop in calcification with concurrent up-regulation of Ca-ATPase and Mg-ATPase, implying increased energy expenditure on calcification. Consequently, asexual budding rates decreased by 50% under fluctuating OA. These results suggest that diel pCO2 oscillations could modify the physiological responses and potentially alter the energy budget of coral recruits under future OA, and that fluctuating OA is more energetically expensive for the maintenance of coral recruits than stable OA.
Project description:Rising atmospheric CO2 is causing the oceans to both warm and acidify, which could reduce the calcification rates of corals globally. Successful coral recruitment and high rates of juvenile calcification are critical to the replenishment and ultimate viability of coral reef ecosystems. Although elevated Pco2 (partial pressure of CO2) has been shown to reduce the skeletal weight of coral recruits, the structural changes caused by acidification during initial skeletal deposition are unknown. We show, using high-resolution three-dimensional x-ray microscopy, that ocean acidification (Pco2 ~900 ?atm, pH ~7.7) not only causes reduced overall mineral deposition but also a deformed and porous skeletal structure in newly settled coral recruits. In contrast, elevated temperature (+3°C) had little effect on skeletal formation except to partially mitigate the effects of elevated Pco2. The striking structural deformities we observed show that new recruits are at significant risk, being unable to effectively build their skeletons in the Pco2 conditions predicted to occur for open ocean surface waters under a "business-as-usual" emissions scenario [RCP (representative concentration pathway) 8.5] by the year 2100.
Project description:Dinoflagellates from the Symbiodiniaceae family and corals have an ecologically important endosymbiotic relationship. Scleractinian corals cannot survive for long periods without their symbionts. These algae, also known as zooxanthellae, on the other hand, thrives outside the coral cells. The free-living populations of zooxanthellae are essential for the resilience of the coral to environmental stressors such as temperature anomalies and ocean acidification. Yet, little is known about how ocean acidification may affect the free-living zooxanthellae. In this study we aimed to test morphological, physiological and biochemical responses of zooxanthellae from the Symbiodinium genus isolated from the coral Mussismilia braziliensis, endemic to the Brazilian coast, to acidification led by increased atmospheric CO2. We tested whether photosynthetic yield, cell ultrastructure, cell density and lipid profile would change after up to 16 days of exposure to pH 7.5 in an atmospheric pCO2 of 1633 ?atm. Photosynthetic yield and cell density were negatively affected and chloroplasts showed vesiculated thylakoids, indicating morphological damage. Moreover, Symbiodinium fatty acid profile drastically changed in acidified condition, showing lower polyunsaturated fatty acids and higher saturated fatty acids contents, when compared to the control, non-acidified condition. These results show that seawater acidification as an only stressor causes significant changes in the physiology, biochemistry and ultrastructure of free-living Symbiodinium.
Project description: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.
Project description:Rising temperatures and ocean acidification driven by anthropogenic carbon emissions threaten both tropical and temperate corals. However, the synergistic effect of these stressors on coral physiology is still poorly understood, in particular for cold-water corals. This study assessed changes in key physiological parameters (calcification, respiration and ammonium excretion) of the widespread cold-water coral Desmophyllum dianthus maintained for ?8 months at two temperatures (ambient 12 °C and elevated 15 °C) and two pCO2 conditions (ambient 390 ppm and elevated 750 ppm). At ambient temperatures no change in instantaneous calcification, respiration or ammonium excretion rates was observed at either pCO2 levels. Conversely, elevated temperature (15 °C) significantly reduced calcification rates, and combined elevated temperature and pCO2 significantly reduced respiration rates. Changes in the ratio of respired oxygen to excreted nitrogen (O:N), which provides information on the main sources of energy being metabolized, indicated a shift from mixed use of protein and carbohydrate/lipid as metabolic substrates under control conditions, to less efficient protein-dominated catabolism under both stressors. Overall, this study shows that the physiology of D. dianthus is more sensitive to thermal than pCO2 stress, and that the predicted combination of rising temperatures and ocean acidification in the coming decades may severely impact this cold-water coral species.
Project description: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 ?atm) and treatment (29.0°C and pCO2 of 750 ?atm) 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.
Project description:Atmospheric pCO2 is predicted to rise from 400 to 900?ppm by year 2100, causing seawater temperature to increase by 1-4?°C and pH to decrease by 0.1-0.3. Sixty-day experiments were conducted to investigate the independent and combined impacts of acidification (pCO2?=?424-426, 888-940?ppm-v) and warming (T?=?28, 32?°C) on calcification rate and skeletal morphology of the abundant and widespread Caribbean reef-building scleractinian coral Siderastrea siderea. Hierarchical linear mixed-effects modelling reveals that coral calcification rate was negatively impacted by both warming and acidification, with their combined effects yielding the most deleterious impact. Negative effects of warming (32?°C/424?ppm-v) and high-temperature acidification (32?°C/940?ppm-v) on calcification rate were apparent across both 30-day intervals of the experiment, while effects of low-temperature acidification (28?°C/888?ppm-v) were not apparent until the second 30-day interval-indicating delayed onset of acidification effects at lower temperatures. Notably, two measures of coral skeletal morphology-corallite height and corallite infilling-were negatively impacted by next-century acidification, but not by next-century warming. Therefore, while next-century ocean acidification and warming will reduce the rate at which corals build their skeletons, next-century acidification will also modify the morphology and, potentially, function of coral skeletons.
Project description:Ocean acidification (OA) is expected to negatively affect coral reefs, however little is known about how OA will change the coral-algal symbiosis on which reefs ultimately depend. This study investigated whether there would be differences in coral Symbiodinium types in response to OA, potentially improving coral performance. We used denaturing gradient gel electrophoresis (DGGE) of the internal transcribed spacer 2 (ITS2) region of ribosomal DNA to investigate the dominant types of Symbiodinium associating with six species of scleractinian coral that were exposed to elevated partial pressures of carbon dioxide (pCO2) in situ from settlement and throughout their lives. The study was conducted at three naturally occurring volcanic CO2 seeps (pCO2 ?500 to 900 ppm, pHTotal 7.8 - 7.9) and adjacent control areas (pCO2 ?390 ppm, pHTotal ?8.0 - 8.05) in Papua New Guinea. The Symbiodinium associated with corals living in an extreme seep site (pCO2 >1000 ppm) were also examined. Ten clade C types and three clade D types dominated the 443 coral samples. Symbiodinium types strongly contrasted between coral species, however, no differences were observed due to CO2 exposure. Within five species, 85 - 95% of samples exhibited the same Symbiodinium type across all sites, with remaining rare types having no patterns attributable to CO2 exposure. The sixth species of coral displayed site specific differences in Symbiodinium types, unrelated to CO2 exposure. Symbiodinium types from the coral inhabiting the extreme CO2 seep site were found commonly throughout the moderate seeps and control areas. Our finding that symbiotic associations did not change in response to CO2 exposure suggest that, within the six coral hosts, none of the investigated 13 clade C and D Symbiodinium types had a selective advantage at high pCO2. Acclimatisation through changing symbiotic association therefore does not seem to be an option for Indo-Pacific corals to deal with future OA.
Project description:Coral reef ecosystems are based on coral-zooxanthellae symbiosis. During the initiation of symbiosis, majority of corals acquire their own zooxanthellae (specifically from the dinoflagellate genus Symbiodinium) from surrounding environments. The mechanisms underlying the initial establishment of symbiosis have attracted much interest, and numerous field and laboratory experiments have been conducted to elucidate this establishment. However, it is still unclear whether the host corals selectively or randomly acquire their symbionts from surrounding environments. To address this issue, we initially compared genetic compositions of Symbiodinium within naturally settled about 2-week-old Acropora coral juveniles (recruits) and those in the adjacent seawater as the potential symbiont source. We then performed infection tests using several types of Symbiodinium culture strains and apo-symbiotic (does not have Symbiodinium cells yet) Acropora coral larvae. Our field observations indicated apparent preference toward specific Symbiodinium genotypes (A1 and D1-4) within the recruits, despite a rich abundance of other Symbiodinium in the environmental population pool. Laboratory experiments were in accordance with this field observation: Symbiodinium strains of type A1 and D1-4 showed higher infection rates for Acropora larvae than other genotype strains, even when supplied at lower cell densities. Subsequent attraction tests revealed that three Symbiodinium strains were attracted toward Acropora larvae, and within them, only A1 and D1-4 strains were acquired by the larvae. Another three strains did not intrinsically approach to the larvae. These findings suggest the initial establishment of corals-Symbiodinium symbiosis is not random, and the infection mechanism appeared to comprise two steps: initial attraction step and subsequent selective uptake by the coral.
Project description:Anthropogenic increases in atmospheric CO2 over this century are predicted to cause global average surface ocean pH to decline by 0.1-0.3 pH units and sea surface temperature to increase by 1-4°C. We conducted controlled laboratory experiments to investigate the impacts of CO2-induced ocean acidification (pCO2 = 324, 477, 604, 2553 µatm) and warming (25, 28, 32°C) on the calcification rate of the zooxanthellate scleractinian coral Siderastrea siderea, a widespread, abundant and keystone reef-builder in the Caribbean Sea. We show that both acidification and warming cause a parabolic response in the calcification rate within this coral species. Moderate increases in pCO2 and warming, relative to near-present-day values, enhanced coral calcification, with calcification rates declining under the highest pCO2 and thermal conditions. Equivalent responses to acidification and warming were exhibited by colonies across reef zones and the parabolic nature of the corals' response to these stressors was evident across all three of the experiment's 30-day observational intervals. Furthermore, the warming projected by the Intergovernmental Panel on Climate Change for the end of the twenty-first century caused a fivefold decrease in the rate of coral calcification, while the acidification projected for the same interval had no statistically significant impact on the calcification rate-suggesting that ocean warming poses a more immediate threat than acidification for this important coral species.