No abstract

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 term "microbiome" was first coined in 1988 and given the definition of a characteristic microbial community occupying a reasonably well defined habitat which has distinct physio-chemical properties. A more recent term has also emerged, taking this one step further and focusing on diseases in host organisms. The "pathobiome" breaks down the concept of "one pathogen = one disease" and highlights the role of the microbiome, more specifically certain members within the microbiome, in causing pathogenesis. The development of next generation sequencing has allowed large data sets to be amassed describing the microbial communities of many organisms and the field of coral biology is no exception. However, the choices made in the analytical process and the interpretation of these data can significantly affect the outcome and the overall conclusions drawn. In this review we explore the implications of these difficulties, as well as highlighting analytical tools developed in other research fields (such as network analysis) which hold substantial potential in helping to develop a deeper understanding of the role of the microbiome in disease in corals. We also make the case that standardization of methods will substantially improve the collective gain in knowledge across research groups.

Tropical coral reefs cover only 0.1% of the seafloor yet provide habitat for >30% of all marine multicellular species 1 . Ecosystem services delivered through healthy tropical reefs are economically valued at around US $9,900,000 million per year 2 and sustain almost a billion people [3][4][5] . Despite their importance, catastrophic global loss of coral reefs owing to anthropogenic activity is fast becoming a reality 6 . For example, the 2015-2018 global coral bleaching event affected 74% of reefs worldwide, with >30% of coral cover lost on the Great Barrier Reef alone 7 . Additionally, coral cover in the Florida Reef Tract has declined by upwards of 90% over the last 50 years [8][9][10][11] .A global contributing factor to reef degradation is coral bleaching 12,13 . Without their microalgal symbionts (Fig. 1), corals lose their primary source of nutrition, leading to starvation, reduced fecundity, and reduced growth, often resulting in widespread coral mortality 14,15 . Trajectories for coral reefs under present CO 2 emission scenarios are dire, with 60% of all remaining coral reefs critically threatened, and 98% exposed to environmental conditions above the current thresholds considered necessary to maintain ecosystem function as soon as 2030 (reF. 16 ). The impact of ocean warming is exacerbated by the effects of ocean acidification 17 , deoxygenation 18 , and salinity changes 19 . Combined with local factors such as overfishing, coastal development, disturbance of the nutrient environment (water quality), and disease or predator outbreaks, the interrelated cumulative impacts all contribute to reduction in coral cover and declining reef ecosystem health [20][21][22][23][24][25][26][27] .Given the rate and extent at which climate change unfolds 28 , a widespread and shared concern is that the rate of environmental change could outpace the ability of coral holobionts to adapt to the changing environment 29 , concomitant with the increasing loss of coral reef cover 30 . Global mitigation of CO 2 emissions is unquestionably needed to stem the rate of declining reef health [30][31][32] . However, biological, ecological and socio-economic adaptations are critical partners to preserve reefs and delay the loss of coral populations until carbon mitigation is effectively implemented 30 . Reef protection through Marine Protected Areas and management practices reduces how local stressors compound global climate change impacts 27,31 . Nevertheless, the current state of reefs and their predicted further decline have sparked initiatives to prioritize reefs or corals that are less vulnerable to climate change and best positioned for regenerating other degraded reefs in the future [33][34][35] . Coral bleachingDiscolouration of coral tissue due to the loss of microalgal symbionts triggered by climate change-induced ocean warming and thermal stress anomalies.

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.