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.

Coral physiology and microbiome dynamics under combined warming and ocean acidification

Abstract Corals live in a complex, multipartite symbiosis with diverse microbes across kingdoms, some of which are implicated in vital functions, such as those related to resilience against climate change. However, knowledge gaps and technical challenges limit our understanding of the nature and functional significance of complex symbiotic relationships within corals. Here, we provide an overview of the complexity of the coral microbiome focusing on taxonomic diversity and functions of well-studied and cryptic microbes. Mining the coral literature indicate that while corals collectively harbour a third of all marine bacterial phyla, known bacterial symbionts and antagonists of corals represent a minute fraction of this diversity and that these taxa cluster into select genera, suggesting selective evolutionary mechanisms enabled these bacteria to gain a niche within the holobiont. Recent advances in coral microbiome research aimed at leveraging microbiome manipulation to increase coral’s fitness to help mitigate heat stress-related mortality are discussed. Then, insights into the potential mechanisms through which microbiota can communicate with and modify host responses are examined by describing known recognition patterns, potential microbially derived coral epigenome effector proteins and coral gene regulation. Finally, the power of omics tools used to study corals are highlighted with emphasis on an integrated host–microbiota multiomics framework to understand the underlying mechanisms during symbiosis and climate change-driven dysbiosis.

/pdf/the-coral-microbiome-towards-an-understanding-of-the-fnrl1gwx.pdf

The coral microbiome: towards an understanding of the molecular mechanisms of coral–microbiota interactions

Corals are the main primary producers of coral reefs and build the three-dimensional reef structure that provides habitat to more than 25% of all marine eukaryotes. They harbor a complex consortium of microorganisms, including bacteria, archaea, fungi, viruses, and protists, which they rely on for their survival. The symbiosis between corals and bacteria is poorly studied, and their symbiotic relationships with intracellular bacteria are only just beginning to be acknowledged. In this review, we emphasize the importance of characterizing intracellular bacteria associated with corals and explore how successful approaches used to study such microorganisms in other systems could be adapted for research on corals. We propose a framework for the description, identification, and functional characterization of coral-associated intracellular bacterial symbionts. Finally, we highlight the possible value of intracellular bacteria in microbiome manipulation and mitigating coral bleaching.

Intracellular Bacterial Symbionts in Corals: Challenges and Future Directions.

In the past 20 years, a new concept has slowly emerged and expanded to various domains of marine biology research: the holobiont. A holobiont describes the consortium formed by a eukaryotic host and its associated microorganisms including bacteria, archaea, protists, microalgae, fungi and viruses. From coral reefs to the deep-sea, symbiotic relationships and host-microbiome interactions are omnipresent and central to the health of marine ecosystems. Studying marine organisms under the light of the holobiont is a new paradigm that impacts many aspects of marine sciences. This approach is an innovative way of understanding the complex functioning of marine organisms, their evolution, their ecological roles within their ecosystems, and their adaptation to face environmental changes. This review offers a broad insight into key concepts of holobiont studies and into the current knowledge of marine model holobionts. Firstly, the history of the holobiont concept and the expansion of its use from evolutionary sciences to other fields of marine biology will be discussed. Then, the ecology and physiology of marine holobionts will be investigated through the examples of corals and sponges. We will discuss the impacts of environmental change on organisms at the holobiont level and how microbiomes contribute to the resilience and/or vulnerability of their host in the face of environmental stressors. Finally, we will conclude with the development of new technologies, holistic approaches and future prospects for conservation biology surrounding marine holobionts.

/pdf/corals-and-sponges-under-the-light-of-the-holobiont-concept-vrd9laglvv.pdf

Corals and Sponges Under the Light of the Holobiont Concept: How Microbiomes Underpin Our Understanding of Marine Ecosystems

Abstract Symbiodiniaceae form associations with extra- and intracellular bacterial symbionts, both in culture and in symbiosis with corals. Bacterial associates can regulate Symbiodiniaceae fitness in terms of growth, calcification and photophysiology. However, the influence of these bacteria on interactive stressors, such as temperature and light, which are known to influence Symbiodiniaceae physiology, remains unclear. Here, we examined the photophysiological response of two Symbiodiniaceae species ( Symbiodinium microadriaticum and Breviolum minutum ) cultured under acute temperature and light stress with specific bacterial partners from their microbiome ( Labrenzia ( Roseibium ) alexandrii , Marinobacter adhaerens or Muricauda aquimarina ). Overall, bacterial presence positively impacted Symbiodiniaceae core photosynthetic health (photosystem II [PSII] quantum yield) and photoprotective capacity (non-photochemical quenching; NPQ) compared to cultures with all extracellular bacteria removed, although specific benefits were variable across Symbiodiniaceae genera and growth phase. Symbiodiniaceae co-cultured with M. aquimarina displayed an inverse NPQ response under high temperatures and light, and those with L. alexandrii demonstrated a lowered threshold for induction of NPQ, potentially through the provision of antioxidant compounds such as zeaxanthin (produced by Muricauda spp . ) and dimethylsulfoniopropionate (DMSP; produced by this strain of L. alexandrii ). Our co-culture approach empirically demonstrates the benefits bacteria can deliver to Symbiodiniaceae photochemical performance, providing evidence that bacterial associates can play important functional roles for Symbiodiniaceae. 

Symbiodiniaceae photophysiology and stress resilience is enhanced by microbial associations

Phycosphere is the region where algal exudates influence microbial communities. Since the term was coined, research has been focused on understanding free-living-phytoplankton and bacteria interactions. Coral-Symbiodiniaceae symbiosis and its associated microbiomes have also been widely studied due to the increasing number of global and local threats endangering coral reefs worldwide. Nevertheless, little is known about the specific interactions between Symbiodiniaceae and bacterial communities within a coral host. In this review, we focus on Symbiodiniaceae-bacteria relationships, occurring in a zone we call here ‘Symbiodiniaceae phycosphere’, within the coral holobiont, in view of 1) identifying and outlining Symbiodiniaceae-bacteria interactions; 2) highlighting interkingdom signaling among phycosphere partners and 3) characterizing microbiome diversity and its relevance to ‘Symbiodiniaceae phycosphere’ as an adaptability generator. Since free-living Symbiodiniaceae are associated with a diverse, structured and dynamic microbial community that are attracted by chemotaxis to the microalgae exudates’ gradient, the maintenance of this gradient and its effect on the microbiota inside the coral host is a must. Here, we raise evidence that sustains the ‘Symbiodiniaceae phycosphere’ as a relevant portion of the coral holobiont, where essential roles in the holobiont’s fitness, acclimatization, adaptability and survival are presented, both in homeostatic and adverse conditions.

Insights into ‘Symbiodiniaceae phycosphere’ in a coral holobiont

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Insights into ‘Symbiodiniaceae phycosphere’ in a coral holobiont