Significance: Flexibility in the endosymbiotic Symbiodinium community could provide reef-building corals with the capacity to survive environmental change, but this may be restricted to compatible host-symbiont combinations. Therefore, determining the underlying molecular, cellular, and physiological processes of symbiont compatibility is of critical importance for elucidating the resilience and adaptability of coral reefs. We coupled gene expression data with high-throughput metabolite profiling to compare the effects on the sea anemone Aiptasia when colonized by the thermally tolerant, opportunistic, but comparatively unproductive Symbiodinium trenchii vs. the regular symbiont species, Symbiodinium minutum . This powerful approach revealed strong evidence that optimal nutritional exchange and the response to intracellular oxidative stress are important determinants in the success of novel cnidarian-dinoflagellate symbioses.

Coral bleaching is the single largest global threat to coral reefs worldwide. Integrating the diverse body of work on coral bleaching is critical to understanding and combating this global problem. Yet investigating the drivers, patterns, and processes of coral bleaching poses a major challenge. A recent review of published experiments revealed a wide range of experimental variables used across studies. Such a wide range of approaches enhances discovery, but without full transparency in the experimental and analytical methods used, can also make comparisons among studies challenging. To increase comparability but not stifle innovation, we propose a common framework for coral bleaching experiments that includes consideration of coral provenance, experimental conditions, and husbandry. For example, reporting the number of genets used, collection site conditions, the experimental temperature offset(s) from the maximum monthly mean (MMM) of the collection site, experimental light conditions, flow, and the feeding regime will greatly facilitate comparability across studies. Similarly, quantifying common response variables of endosymbiont (Symbiodiniaceae) and holobiont phenotypes (i.e., color, chlorophyll, endosymbiont cell density, mortality, and skeletal growth) could further facilitate cross‐study comparisons. While no single bleaching experiment can provide the data necessary to determine global coral responses of all corals to current and future ocean warming, linking studies through a common framework as outlined here, would help increase comparability among experiments, facilitate synthetic insights into the causes and underlying mechanisms of coral bleaching, and reveal unique bleaching responses among genets, species, and regions. Such a collaborative framework that fosters transparency in methods used would strengthen comparisons among studies that can help inform coral reef management and facilitate conservation strategies to mitigate coral bleaching worldwide.

Summary: The intimate relationship between scleractinian corals and their associated microorganisms is fundamental to healthy coral reef ecosystems. Coral‐associated microbes (Symbiodiniaceae and other protists, bacteria, archaea, fungi and viruses) support coral health and resilience through metabolite transfer, inter‐partner signalling, and genetic exchange. However, much of our understanding of the coral holobiont relationship has come from studies that have investigated either coral‐Symbiodiniaceae or coral‐bacteria interactions in isolation, while relatively little research has focused on other ecological and metabolic interactions potentially occurring within the coral multi‐partner symbiotic network. Recent evidences of intimate coupling between phytoplankton and bacteria have demonstrated that obligate resource exchange between partners fundamentally drives their ecological success. Here, we posit that similar associations with bacterial consortia regulate Symbiodiniaceae productivity and are in turn central to the health of corals. Indeed, we propose that this bacteria‐Symbiodiniaceae‐coral relationship underpins the coral holobiont's nutrition, stress tolerance and potentially influences the future survival of coral reef ecosystems under changing environmental conditions. Resolving Symbiodiniaceae‐bacteria associations is therefore a logical next step towards understanding the complex multi‐partner interactions occurring in the coral holobiont.

Most lost fishing gear is made of non-biodegradable plastics that may sink to the sea floor or drift around in currents. It may remain unnoticed until it shows up on coral reefs, beaches and in other coastal habitats. Stony corals have fragile skeletons and soft tissues that can easily become damaged when they get in contact with lost fishing gear. During a dive survey around Koh Tao, a small island in the Gulf of Thailand, the impact of lost fishing gear (nets, ropes, cages, lines) was studied on corals representing six different growth forms: branching, encrusting, foliaceous, free-living, laminar, and massive. Most gear (>95%) contained plastic. Besides absence of damage (ND), three categories of coral damage were assessed: fresh tissue loss (FTL), tissue loss with algal growth (TLAG), and fragmentation (FR). The position of the corals in relation to the fishing gear was recorded as either growing underneath (Un) or on top (On), whereas corals adjacent to the gear (Ad) were used as controls. Nets formed the dominant type of lost gear, followed by ropes, lines and cages, respectively. Branching corals were most commonly found in contact with the gear and also around it. Tubastraea micranthus was the most commonly encountered coral species, either Un, On, or Ad. Corals underneath gear showed most damage, which predominantly consisted of tissue loss. Fragmentation was less common than expected, which may be related to the low fragility of T. micranthus as dominant branching species. Even if nets serve as substrate for corals, it is recommended to remove them from reefs, where they form a major component of the plastic pollution and cause damage to corals and other reef organisms.

Metabolite exchange is fundamental to the viability of the cnidarian–Symbiodiniaceae symbiosis and survival of coral reefs. Coral holobiont tolerance to environmental change might be achieved through changes in Symbiodiniaceae species composition, but differences in the metabolites supplied by different Symbiodiniaceae species could influence holobiont fitness. Using ¹³ C stable-isotope labelling coupled to gas chromatography–mass spectrometry, we characterized newly fixed carbon fate in the model cnidarian Exaiptasia pallida (Aiptasia) when experimentally colonized with either native Breviolum minutum or non-native Durusdinium trenchii . Relative to anemones containing B. minutum , D. trenchii -colonized hosts exhibited a 4.5-fold reduction in ¹³ C-labelled glucose and reduced abundance and diversity of ¹³ C-labelled carbohydrates and lipogenesis precursors, indicating symbiont species-specific modifications to carbohydrate availability and lipid storage. Mapping carbon fate also revealed significant alterations to host molecular signalling pathways. In particular, D. trenchii- colonized hosts exhibited a 40-fold reduction in ¹³ C-labelled scyllo -inositol, a potential interpartner signalling molecule in symbiosis specificity. ¹³ C-labelling also highlighted differential antioxidant- and ammonium-producing pathway activities, suggesting physiological responses to different symbiont species. Such differences in symbiont metabolite contribution and host utilization may limit the proliferation of stress-driven symbioses; this contributes valuable information towards future scenarios that select in favour of less-competent symbionts in response to environmental change.

Experimental manipulation of the symbiosis between cnidarians and photosynthetic dinoflagellates (Symbiodinium spp.) is critical to advance understanding of the cellular mechanisms involved in host–symbiont interactions, and overall coral reef ecology. The anemone Aiptasia sp. is a model for the cnidarian-dinoflagellate symbiosis, and notably it can be rendered aposymbiotic (i.e. dinoflagellate-free) and re-infected with a range of Symbiodinium types. Various methods exist for generating aposymbiotic hosts, however they can be hugely time-consuming and not wholly effective. Here, we optimise a method using menthol for production of aposymbiotic Aiptasia. The menthol treatment produced aposymbiotic hosts within just four weeks (97–100% symbiont loss), which was maintained long after treatment when anemones were held under a standard light/dark cycle. The ability of Aiptasia to form a stable symbiosis appeared unaffected by menthol exposure, as demonstrated by successful symbiosis re-establishment when experimentally re-infected. Furthermore, there was no significant impact on photosynthetic or respiratory performance of re-infected anemones.