Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality.

The use of Beneficial Microorganisms for Corals (BMCs) has been proposed recently as a tool for the improvement of coral health, with knowledge in this research topic advancing rapidly. BMCs are defined as consortia of microorganisms that contribute to coral health through mechanisms that include ( a) promoting coral nutrition and growth, ( b) mitigating stress and impacts of toxic compounds, ( c) deterring pathogens, and ( d) benefiting early life-stage development. Here, we review the current proposed BMC approach and outline the studies that have proven its potential to increase coral resilience to stress. We revisit and expand the list of putative beneficial microorganisms associated with corals and their proposed mechanisms that facilitate improved host performance. Further, we discuss the caveats and bottlenecks affecting the efficacy of BMCs and close by focusing on the next steps to facilitate application at larger scales that can improve outcomes for corals and reefs globally. Expected final online publication date for the Annual Review of Animal Biosciences, Volume 9 is February 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Our paper is the first study to synthesize currently available but decentralized data of cultured microbes associated with corals. We were able to collate 3,055 isolates across a number of published studies and unpublished collections from various laboratories and researchers around the world.

Coral reefs are threatened by climate change on a global scale with thermal stress events and mass coral bleaching being widely reported. The reefs off the east coast of Brazil (and other turbid areas) have, however, historically escaped such thermal stress events, with relatively low levels of background coral mortality (5-10%). This has recently changed. Here we show that, in 2019, degree heating weeks (DHW) of 19.65 coincided with catastrophic declines in coral cover, especially in the major reef building hydrocoral Millepora alcicornis. The decline was due to bleaching associated with exposure to high temperature stress culminating in DHW values exceeding 15 for a period of 50 days. At two independent sites, surveys showed upwards of 83.5 ± 9.0 and 89.1 ± 3.9% mortality, and a third site showed relatively lower (albeit still high) mortality rates of 43.3 ± 12.0%. The mass die-off in 2019 is unprecedented in the South Atlantic reefs and coincides with increased heating events.

Bacteria associated with coral hosts are diverse and abundant, with recent studies suggesting involvement of these symbionts in host resilience to anthropogenic stress. Despite the putative importance of bacteria, the work dedicated to culturing coral-associated bacteria has received little attention. Combining published and unpublished data, here we report a comprehensive overview of the diversity and function of culturable, coral-associated bacteria. A total of 3055 isolates from 52 studies were considered by our meta-survey. Of these, 1045 had full length 16S rRNA gene sequences, spanning 138 formally described and 12 putatively novel bacterial genera across the Proteobacteria, Firmicutes, Bacteroidetes, and Actinobacteria phyla. We performed comparative genomic analysis using the available genomes of 74 strains and identified potential signatures of beneficial bacterial-coral symbioses among them. Our analysis revealed >400 biosynthetic gene clusters that underlie the biosynthesis of antioxidant, antimicrobial, cytotoxic, and other secondary metabolites. Moreover, we uncovered genomic features - not previously described for coral-bacterial symbioses - involved in host colonization and host-symbiont recognition, antiviral defence mechanisms, and/or integrated metabolic interactions, which we suggest as novel targets for the screening of coral probiotics. Our results highlight the importance of bacterial cultures to elucidate coral holobiont functioning, and guide the selection of probiotic candidates to promote coral resilience and improve reef restoration efforts.

Global biodiversity loss and mass extinction of species are two of the most critical environmental issues the world is currently facing, resulting in the disruption of various ecosystems central to environmental functions and human health. Microbiome-targeted interventions, such as probiotics and microbiome transplants, are emerging as potential options to reverse deterioration of biodiversity and increase the resilience of wildlife and ecosystems. However, the implementation of these interventions is urgently needed. We summarize the current concepts, bottlenecks and ethical aspects encompassing the careful and responsible management of ecosystem resources using the microbiome (termed microbiome stewardship) to rehabilitate organisms and ecosystem functions. We propose a real-world application framework to guide environmental and wildlife probiotic applications. This framework details steps that must be taken in the upscaling process while weighing risks against the high toll of inaction. In doing so, we draw parallels with other aspects of contemporary science moving swiftly in the face of urgent global challenges.

Background Beginning in the last century, coral reefs have suffered the consequences of anthropogenic activities, including oil contamination. Chemical remediation methods, such as dispersants, can cause substantial harm to corals and reduce their resilience to stressors. To evaluate the impacts of oil contamination and find potential alternative solutions to chemical dispersants, we conducted a mesocosm experiment with the fire coral Millepora alcicornis, which is sensitive to environmental changes. We exposed M. alcicornis to a realistic oil-spill scenario in which we applied an innovative multi-domain bioremediator consortium (bacteria, filamentous fungi, and yeast) and a chemical dispersant (Corexit® 9500, one of the most widely used dispersants), to assess the effects on host health and host-associated microbial communities. Results The selected multi-domain microbial consortium helped to mitigate the impacts of the oil, substantially degrading the polycyclic aromatic and n-alkane fractions and maintaining the physiological integrity of the corals. Exposure to Corexit 9500 negatively impacted the host physiology and altered the coral-associated microbial community. After exposure, the abundances of certain bacterial genera such as Rugeria and Roseovarius increased, as previously reported in stressed or diseased corals. We also identified several bioindicators of Corexit 9500 in the microbiome. The impact of Corexit 9500 on the coral health and microbial community was far greater than oil alone, killing corals after only 4 days of exposure in the flow-through system. In the treatments with Corexit 9500, the action of the bioremediator consortium could not be observed directly because of the extreme toxicity of the dispersant to M. alcicornis and its associated microbiome. Conclusions Our results emphasize the importance of investigating the host-associated microbiome in order to detect and mitigate the effects of oil contamination on corals and the potential role of microbial mitigation and bioindicators as conservation tools. Chemical dispersants were far more damaging to corals and their associated microbiome than oil, and should not be used close to coral reefs. This study can aid in decision-making to minimize the negative effects of oil and dispersants on coral reefs.

Ocean higher temperature and acidity levels affect its carbonate chemistry, and calcifying organisms that depend on the calcium carbonate saturation state (ΩCaCO3) to build their skeleton may be vulnerable to these changes. Despite their important roles in the marine environment, little is known about the vulnerability of calcareous sponges under these stressors. We performed an acute short-term experiment (9 days) with thermal and pH stresses to explore their effects on the skeleton and microbiome of the calcareous sponge Sycettusa hastifera. We observed that sponge spicules showed no corrosion and no Mg/Ca ratio variation when exposed to stress conditions. However, the outermost spicules were smaller in low pH treatment, although these effects were often diminished when higher temperatures were also applied. In general, the sponges synthesized normally shaped spicules under stress conditions, but the proportion of deformed spicules increased significantly in elevated temperature. In addition, we observed a stable host–microbiome association in which there is microbiome flexibility under thermal and pH stresses with a significantly increase in abundance of some associated bacteria. Our results suggest that S. hastifera has low vulnerability under the future ocean conditions here designed, since it showed indications of resistance that could help them adapt and survive.