Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral–algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral–algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral–algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general. Significance Ocean warming is causing repeated mass coral bleaching, leading to catastrophic losses of coral reefs worldwide. Our ability to slow or revert this decline is hampered by an incomplete understanding of the processes underlying the breakdown of the coral–algal symbiosis. Here, we show that heat stress destabilizes the nutrient cycling between corals and their endosymbiotic algae long before bleaching becomes apparent. Notably, increased metabolic energy demands shift the coral–algal symbiosis from a nitrogen- to a carbon-limited state, reducing translocation and recycling of photosynthetic carbon. This effectively undermines the ecological advantage of harboring algal symbionts and directly contributes to the breakdown of the coral–algal symbiosis during heat stress.

The disruption of the coral–algae symbiosis (coral bleaching) due to rising sea surface temperatures has become an unprecedented global threat to coral reefs. Despite decades of research, our ability to manage mass bleaching events remains hampered by an incomplete mechanistic understanding of the processes involved. In this study, we induced a coral bleaching phenotype in the absence of heat and light stress by adding sugars. The sugar addition resulted in coral symbiotic breakdown accompanied by a fourfold increase of coral‐associated microbial nitrogen fixation. Concomitantly, increased N:P ratios by the coral host and algal symbionts suggest excess availability of nitrogen and a disruption of the nitrogen limitation within the coral holobiont. As nitrogen fixation is similarly stimulated in ocean warming scenarios, here we propose a refined coral bleaching model integrating the cascading effects of stimulated microbial nitrogen fixation. This model highlights the putative role of nitrogen‐fixing microbes in coral holobiont functioning and breakdown.

This document is the work of a team assembled by the International Coral Reef Society (ICRS). The mission of ICRS is to promote the acquisition and dissemination of scientific knowledge to secure the future of coral reefs, including via relevant policy frameworks and decision-making processes. This document seeks to highlight the urgency of taking action to conserve and restore reefs through protection and management measures, to provide a summary of the most relevant and recent natural and social science that provides guidance on these tasks, and to highlight implications of these findings for the numerous discussions and negotiations taking place at the global level.

The importance of Symbiodinium algal endosymbionts and a diverse suite of bacteria for coral holobiont health and functioning are widely acknowledged. Yet, we know surprisingly little about microbial community dynamics and the stability of host‐microbe associations under adverse environmental conditions. To gain insight into the stability of coral host‐microbe associations and holobiont structure, we assessed changes in the community structure of Symbiodinium and bacteria associated with the coral Pocillopora verrucosa under excess organic nutrient conditions. Pocillopora‐associated microbial communities were monitored over 14 days in two independent experiments. We assessed the effect of excess dissolved organic nitrogen (DON) and excess dissolved organic carbon (DOC). Exposure to excess nutrients rapidly affected coral health, resulting in two distinct stress phenotypes: coral bleaching under excess DOC and severe tissue sloughing (>90% tissue loss resulting in host mortality) under excess DON. These phenotypes were accompanied by structural changes in the Symbiodinium community. In contrast, the associated bacterial community remained remarkably stable and was dominated by two Endozoicomonas phylotypes, comprising on average 90% of 16S rRNA gene sequences. This dominance of Endozoicomonas even under conditions of coral bleaching and mortality suggests the bacterial community of P. verrucosa may be rather inflexible and thereby unable to respond or acclimatize to rapid changes in the environment, contrary to what was previously observed in other corals. In this light, our results suggest that coral holobionts might occupy structural landscapes ranging from a highly flexible to a rather inflexible composition with consequences for their ability to respond to environmental change.

Microbial nitrogen fixation (diazotrophy) is a functional trait widely associated with tropical reef-building (scleractinian) corals. While the integral role of nitrogen fixation in coral nutrient dynamics is recognized, its ecological significance across different coral functional groups remains yet to be evaluated. Here we set out to compare molecular and physiological patterns of diazotrophy (i.e., nifH gene abundance and expression as well as nitrogen fixation rates) in two coral families with contrasting trophic strategies: highly heterotrophic, free-living members of the family Fungiidae (Pleuractis granulosa, Ctenactis echinata), and mostly autotrophic coral holobionts with low heterotrophic capacity (Pocilloporidae: Pocillopora verrucosa, Stylophora pistillata). The Fungiidae exhibited low diazotroph abundance (based on nifH gene copy numbers) and activity (based on nifH gene expression and the absence of detectable nitrogen fixation rates). In contrast, the mostly autotrophic Pocilloporidae exhibited nifH gene copy numbers and gene expression two orders of magnitude higher than in the Fungiidae, which coincided with detectable nitrogen fixation activity. Based on these data, we suggest that nitrogen fixation compensates for the low heterotrophic nitrogen uptake in autotrophic corals. Consequently, the ecological importance of diazotrophy in coral holobionts may be determined by the trophic functional group of the host.

Coral reefs in the wider Caribbean declined in hard coral cover by ~80% since the 1970s, but spatiotemporal analyses for sub-regions are lacking. Here, we explored benthic change patterns in the Mexican Caribbean reefs through meta-analysis between 1978 and 2016 including 125 coral reef sites. Findings revealed that hard coral cover decreased from ~26% in the 1970s to 16% in 2016, whereas macroalgae cover increased to ~30% in 2016. Both groups showed high spatiotemporal variability. Hard coral cover declined in total by 12% from 1978 to 2004 but increased again by 5% between 2005 and 2016 indicating some coral recovery after the 2005 mass bleaching event and hurricane impacts. In 2016, more than 80% of studied reefs were dominated by macroalgae, while only 15% were dominated by hard corals. This stands in contrast to 1978 when all reef sites surveyed were dominated by hard corals. This study is among the first within the Caribbean region that reports local recovery in coral cover in the Caribbean, while other Caribbean reefs have failed to recover. Most Mexican Caribbean coral reefs are now no longer dominated by hard corals. In order to prevent further reef degradation, viable and reliable conservation alternatives are required.