Background: Reef-building corals are acutely threatened by ocean warming, calling for active interventions to reduce coral bleaching and mortality. Corals associate with a wide diversity of bacteria which can influence coral health, but knowledge of specific functions that may be beneficial for corals under thermal stress is scant. Under the oxidative stress theory of coral bleaching, bacteria that scavenge reactive oxygen (ROS) or nitrogen species (RNS) are expected to enhance coral thermal resilience. Further, bacterial carbon export might substitute the carbon supply from algal photosymbionts, enhance thermal resilience and facilitate bleaching recovery. To identify probiotic bacterial candidates, we sequenced the genomes of 82 pure-cultured bacteria that were isolated from the emerging coral model Galaxea fascicularis. Results: Genomic analyses showed bacterial isolates were affiliated with 37 genera. Isolates such as Ruegeria, Muricauda and Roseovarius were found to encode genes for the synthesis of the antioxidants mannitol, glutathione, dimethylsulfide, dimethylsulfoniopropionate, zeaxanthin and/or β-carotene. Genes involved in RNS-scavenging were found in many G. fascicularis-associated bacteria, which represents a novel finding for several genera (including Pseudophaeobacter). Transporters that are suggested to export carbon (semiSWEET) were detected in seven isolates, including Pseudovibrio and Roseibium. Further, a range of bacterial strains, including strains of Roseibium and Roseovarius, revealed genomic features that may enhance colonisation and association of bacteria with the coral host, such as secretion systems and eukaryote-like repeat proteins. Conclusions: Our work provides an in-depth genomic analysis of the functional potential of G. fascicularis-associated bacteria and identifies novel combinations of traits that may enhance the coral’s ability to withstand coral bleaching. Identifying and characterising bacteria that are beneficial for corals is critical for the development of effective probiotics that boost coral climate resilience.

Coral reefs are threatened by climate change, because it causes increasingly frequent and severe summer heatwaves, resulting in mass coral bleaching and mortality. Coral bleaching is believed to be driven by an excess production of reactive oxygen (ROS) and nitrogen species (RNS), yet their relative roles during thermal stress remain understudied. Here, we measured ROS and RNS net production, as well as activities of key enzymes involved in ROS scavenging (superoxide dismutase and catalase) and RNS synthesis (nitric oxide synthase) and linked these metrics to physiological measurements of cnidarian holobiont health during thermal stress. We did this for both an established cnidarian model, the sea anemone Exaiptasia diaphana, and an emerging scleractinian model, the coral Galaxea fascicularis, both from the Great Barrier Reef (GBR). Increased ROS production was observed during thermal stress in both species, but it was more apparent in G. fascicularis, which also showed higher levels of physiological stress. RNS did not change in thermally stressed G. fascicularis and decreased in E. diaphana. Our findings in combination with variable ROS levels in previous studies on GBR-sourced E. diaphana suggest G. fascicularis is a more suitable model to study the cellular mechanisms of coral bleaching.

Coral reefs house one-third of all marine species and are of high cultural and socioeconomic importance. However, coral reefs are under dire threat from climate change and other anthropogenic stressors. Climate change is causing coral bleaching, the breakdown of the symbiosis between the coral host and its algal symbionts, often resulting in coral mortality and the deterioration of these valuable ecosystems. While it is essential to counteract the root causes of climate change, it remains urgent to develop coral restoration and conservation methods that will buy time for coral reefs. The manipulation of the bacterial microbiome that is associated with corals has been suggested as one intervention to improve coral climate resilience. Early coral microbiome-manipulation studies, which are aimed at enhancing bleaching tolerance, have shown promising results, but the inoculated bacteria did generally not persist within the coral microbiome. Here, we highlight the importance of long-term incorporation of bacterial inocula into the microbiome of target corals, as repeated inoculations will be too costly and not feasible on large reef systems like the Great Barrier Reef. Therefore, coral microbiome-manipulation studies need to prioritise approaches that can provide sustained coral climate resilience.

A rapid decline of coral reefs is taking place around the world, with climate warming being the biggest driver behind this deterioration. Efforts to increase coral climate resilience via bioengineering methods have thus become urgent, and there is hope that such interventions can help corals and coral reefs survive until a time when no further climate warming occurs and perhaps a future of climate cooling is imaginable. The manipulation of coral-associated bacterial communities is among the less advanced interventions currently being explored. Nevertheless, early findings provide confidence that some level of thermal enhancement can be achieved via the inoculation of corals with beneficial bacteria. The small number of studies available, however, is limited in terms of the traits used to select candidate bacteria and their ability to ascribe host enhancement to specific bacterial taxa and functions. Further, findings to date are unable to decipher whether candidate bacteria integrate stably within the coral microbiome. These shortcomings prevent assessment of the efficacy of bacterial manipulation to enhance the long-term thermal resilience of corals on the reef. Here we summarise the state-of-play of the field and provide recommendations to fast-track this approach via fine-tuning experimental designs and methods.

Thermal variability can render corals stress resistant through a phenomenon coined as “stress-hardening induced by environmental priming”. Fluctuations that involve high temperature peaks have been commonly investigated, however, the effects of a stress-hardening stimulus generated by cold-water pulses has rarely been studied. Offshore island reefs in the Andaman Sea offer an ideal natural setting to study these effects, as cooling water of internal waves induce strong variability with peak intensity in January to June and absence in August to November. While western island shores are exposed to this stimulus, eastern shores remain sheltered. This study examined (1) whether corals from exposed reefs were more heat stress resistant compared to stimulus-sheltered conspecifics and (2) whether this trait can last in the absence of the stimulus. We quantified the thermal stress resistance in two ecologically important coral species, Pocillopora sp. and Porites sp., from the two island shores, during the two seasons. Coral bleaching intensity and photosynthetic efficiency of algal symbionts were measured as response variables after a short-term heat stress assay (24-48 h, 34 °C) to assess thermal stress resistance. Stress responses of all stimulus-exposed corals were either undetectable (during the season of stimulus presence) or very weak (during stimulus absence), while corals from the stimulus-sheltered shore responded strongly to heat stress irrespective of the season. Hence, thermal resistance was overall greater in corals originating from the stimulus-exposed shore, but it was slightly diminished during the season of stimulus absence, emphasizing the relevance of stimulus recurrence in maintaining the resistance trait. We exemplify that the stimulus of fluctuating low temperature pulses successfully induced stress-hardening in corals. This suggests that priming stimuli do not necessarily need to transgress certain upper thermal thresholds, but can also touch on lower thresholds to be effective. Even more, we argue that cooling pulses might represent a safer stress-hardening regime, since warming-stress accumulation can be avoided. More research is required to obtain a better understanding of environmental priming, but current findings should encourage the development of artificial stress-hardening approaches to enhance coral resistance in reef restoration efforts.