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Coral bleaching, caused by the loss of brownish-colored dinoflagellate photosymbionts from the host tissue of reef-building corals, is a major threat to reef survival. Occasionally, bleached corals become exceptionally colorful rather than white. These colors derive from photoprotective green fluorescent protein (GFP)-like pigments produced by the coral host. There is currently no consensus regarding what causes colorful bleaching events and what the consequences for the corals are. Here, we document that colorful bleaching events are a recurring phenomenon in reef regions around the globe. Our analysis of temperature conditions associated with colorful bleaching events suggests that corals develop extreme coloration within 2 to 3 weeks after exposure to mild or temporary heat stress. We demonstrate that the increase of light fluxes in symbiont-depleted tissue promoted by reflection of the incident light from the coral skeleton induces strong expression of the photoprotective coral host pigments. We describe an optical feedback loop involving both partners of the association, discussing that the mitigation of light stress offered by host pigments could facilitate recolonization of bleached tissue by symbionts. Our data indicate that colorful bleaching has the potential to identify local environmental factors, such as nutrient stress, that can exacerbate the impact of elevated temperatures on corals, to indicate the severity of heat stress experienced by corals and to gauge their post-stress recovery potential. VIDEO ABSTRACT. ; The authors thank Alex Thomson (Scottish Association for Marine Science) for collecting the P. lichen high light acclimation data and Ryan Goehrung (University of Washington), Courtney Couch (NOAA), Richard Vevers (The Ocean Agency), Martin Savers (Reefscapers at http://reefscapers.com), Shreya Yadav (Hawaiʻi Institute of Marine Biology), Ed Roberts (Tethys Images), Michael Fox (Woods Hole Oceanographic Institution), Bill McGraw (https://www.newaquatechpanama.com), Tess Moriarty (University of Newcastle), Fanny Houlbreque (Institute de la Recherce pour le Développement), Andy Bruckner (Coral Reef CPR), Chris Jones (Great Barrier Reef Marine Park Authority), Brian Zgliczynski (Scripps Institution of Oceanography), Louise Laing (People4Ocean), and Darren Coker (JCU Townsville) for providing photographs and background information on colorful bleaching events. The authors acknowledge funding from Natural Environmental Research Council (http://www.nerc.ac.uk/; PhD studentship under NE/L002531/1 to E.B.; NE/I01683X/1, NE/K00641X/1, and NE/I012648/1 to J.W. and C.D.), Deutsche Forschungsgemeinschaft (http://www.dfg.de; Wi1990/2-1 to J.W.), ASSEMBLE (to J.W. and C.D.), the European Research Council (http://erc.europa.eu/) under the European Union's Seventh Framework Programme (ERC grant agreement no. 311179 to J.W.), Tropical Marine Centre London, and Tropic Marin, Wartenberg (NERC CASE studentship to E.B.; sponsorship to the Coral Reef Laboratory).
Ocean warming and ocean acidification (OA) are direct consequences of climate change and affect coral reefs worldwide. While the effect of ocean warming manifests itself in increased frequency and severity of coral bleaching, the effects of ocean acidification on corals are less clear. In particular, long-term effects of OA on the bacterial communities associated with corals are largely unknown. In this study, we investigated the effects of ocean acidification on the resident and active microbiome of long-term aquaria-maintained Stylophora pistillata colonies by assessing 16S rRNA gene diversity on the DNA (resident community) and RNA level (active community). Coral colony fragments of S. pistillata were kept in aquaria for 2 years at four different pCO2 levels ranging from current pH conditions to increased acidification scenarios (i.e., pH 7.2, 7.4, 7.8, and 8). We identified 154 bacterial families encompassing 2,047 taxa (OTUs) in the resident and 89 bacterial families including 1,659 OTUs in the active communities. Resident communities were dominated by members of Alteromonadaceae, Flavobacteriaceae, and Colwelliaceae, while active communities were dominated by families Cyclobacteriacea and Amoebophilaceae. Besides the overall differences between resident and active community composition, significant differences were seen between the control (pH 8) and the two lower pH treatments (7.2 and 7.4) in the active community, but only between pH 8 and 7.2 in the resident community. Our analyses revealed profound differences between the resident and active microbial communities, and we found that OA exerted stronger effects on the active community. Further, our results suggest that rDNA- and rRNA-based sequencing should be considered complementary tools to investigate the effects of environmental change on microbial assemblage structure and activity. ; This study was supported by the KAUST Office of Sponsored Research under award no. FCC/1/1973-22-01 and the Center Scientifique de Monaco Research Program, which is supported by the Government of the Principality of Monaco.
Our understanding of the response of reef-building corals to changes in their physical environment is largely based on laboratory experiments, analysis of long-term field data, and model projections. Experimental data provide unique insights into how organisms respond to variation of environmental drivers. However, an assessment of how well experimental conditions cover the breadth of environmental conditions and variability where corals live successfully is missing. Here, we compiled and analyzed a globally distributed dataset of in-situ seasonal and diurnal variability of key environmental drivers (temperature, pCO2, and O2) critical for the growth and livelihood of reef-building corals. Using a meta-analysis approach, we compared the variability of environmental conditions assayed in coral experimental studies to current and projected conditions in their natural habitats. We found that annual temperature profiles projected for the end of the 21st century were characterized by distributional shifts in temperatures with warmer winters and longer warm periods in the summer, not just peak temperatures. Furthermore, short-term hourly fluctuations of temperature and pCO2 may regularly expose corals to conditions beyond the projected average increases for the end of the 21st century. Coral reef sites varied in the degree of coupling between temperature, pCO2, and dissolved O2, which warrants site-specific, differentiated experimental approaches depending on the local hydrography and influence of biological processes on the carbonate system and O2 availability. Our analysis highlights that a large portion of the natural environmental variability at short and long timescales is underexplored in experimental designs, which may provide a path to extend our understanding on the response of corals to global climate change. ; This study was conducted as part of a competitive research funding grant by the Red Sea Research Center of King Abdullah University of Science and Technology awarded to AA, NG, SK, SSR, and MZ. TLF was supported by the Swiss National Science Foundation (198897), the Swiss National Supercomputing Centre, and the European Union's Horizon 2020 research and innovation program under grant agreement no. 820989 (project COMFORT, "Our common future ocean in the Earth system - quantifying coupled cycles of carbon, oxygen, and nutrients for determining and achieving safe operating spaces with respect to tipping points") and grant agreement no. 862923 (project AtlantECO, "Atlantic Ecosystems Assessment, Forecasting & Sustainability"). ; Peer reviewed