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Abstract Coral bleaching events from thermal stress are increasing globally in duration, frequency, and intensity. While bleaching can cause mortality, some corals survive, reacquire symbionts, and recover. We experimentally bleachedMontipora capitatato examine molecular and physiological differences between corals that recover (resilient) and those that die (susceptible). Corals were collected and monitored for eight months post-bleaching to identify genets with long-term resilience. Using an integrated systems-biology approach that included quantitative proteomics, 16S rRNA sequencing to characterize the coral microbiome, total coral lipids, symbiont community composition and density, we explored molecular-level mechanisms of tolerance in corals pre- and post-bleaching. Prior to thermal stress, resilient corals have a more diverse microbiome and abundant proteins essential for carbon acquisition, symbiont retention, and pathogen resistance. Protein signatures of susceptible corals showed early symbiont rejection and utilized urea for carbon and nitrogen. Our results reveal molecular factors for surviving bleaching events and identify diagnostic protein biomarkers for reef management and restoration. 

Abstract The genomes of mitochondria and chloroplasts contain ribosomal RNA (rRNA) genes, reflecting their ancestry as free-living bacteria. These organellar rRNAs are often amplified in microbiome studies of animals and plants. If identified, they can be discarded, merely reducing sequencing depth. However, we identify certain high-abundance organeller RNAs not identified by common pipelines, which may compromise statistical analysis of microbiome structure and diversity. We quantified this by reanalyzing 7459 samples from seven 16S rRNA studies, including microbiomes from 927 unique animal genera. We find that under-annotation of cryptic mitochondrial and chloroplast reads affects multiple of these large-scale cross-species microbiome comparisons, and varies between host species, biasing comparisons. We offer a straightforward solution: supplementing existing taxonomies with diverse organelle rRNA sequences. This resolves up to 97% of unique unclassified sequences in some entire studies as mitochondrial (14% averaged across all studies), without increasing false positive annotations in mitochondria-free mock communities. Improved annotation decreases the proportion of unknown sequences by ≥10-fold in 2262 of 7459 samples (30%), spanning five of seven major studies examined. We recommend leveraging organelle sequence diversity to better identify organelle gene sequences in microbiome studies, and provide code, data resources and tutorials that implement this approach. 

Abstract Warming ocean temperatures are severely compromising the health and resilience of coral reefs worldwide. Coral bleaching can affect coral physiology and the energy available for corals to reproduce. Mechanisms associated with reproductive allocation in corals are poorly understood, especially after a bleaching event occurs. Using isotopic labeling techniques, we traced the acquisition and allocation of carbon from adults to gametes by autotrophy and heterotrophy in previously bleached and non-bleachedMontipora capitataandPorites compressacorals. Experiments revealed that both species: (1) relied only on autotrophy to allocate carbon to gametes, while heterotrophy was less relied upon as a carbon source; (2) experienced a trade-off with less carbon available for adult tissues when provisioning gametes, especially when previously bleached; and (3) used different strategies for allocating carbon to gametes. Over time,M. capitataallocated 10% more carbon to gametes despite bleaching by limiting the allocation of carbon to adult tissues, with 50–80% less carbon allocated to bleached compared to non-bleached colonies. Over the same time period,P. compressamaintained carbon allocation to adult tissues, before allocating carbon to gametes. Our study highlights the importance of autotrophy for carbon allocation from adult corals to gametes, and species-specific differences in carbon allocation depending on bleaching susceptibility. 

Abstract Coral diseases have increased in frequency and intensity around the tropics worldwide. However, in many cases, little is known about their etiology.Montiporawhite syndrome (MWS) is a common disease affecting the coralMontipora capitata, a major reef builder in Hawai'i. ChronicMontiporawhite syndrome (cMWS) is a slow‐moving form of the disease that affectsM. capitatathroughout the year. The effects of this chronic disease on coral immunology and microbiology are currently unknown. In this study, we use prophenoloxidase immune assays and 16S rRNA gene amplicon sequencing to characterize the microbiome and immunological response associated with cMWS. Our results show that immunological and microbiological responses are highly localized. Relative to diseased samples, apparently healthy portions of cMWS corals differed in immune activity and in the relative abundance of microbial taxa. Coral tissues with cMWS showed decreased tyrosinase‐type catecholase and tyrosinase‐type cresolase activity and increased laccase‐type activity. Catecholase and cresolase activity were negatively correlated across all tissue types with microbiome richness. The localized effect of cMWS on coral microbiology and immunology is probably an important reason for the slow progression of the disease. This local confinement may facilitate interventions that focus on localized treatments on tissue types. This study provides an important baseline to understand the interplay between the microbiome and immune system and the mechanisms used by corals to manage chronic microbial perturbations associated with white syndrome. 

Abstract 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. 

Identifying processes that promote coral reef recovery and resilience is crucial as ocean warming becomes more frequent and severe. Sexual reproduction is essential for the replenishment of coral populations and maintenance of genetic diversity; however, the ability for corals to reproduce may be impaired by marine heatwaves that cause coral bleaching. In 2014 and 2015, the Hawaiian Islands experienced coral bleaching with differential bleaching susceptibility in the speciesMontipora capitata, a dominant reef-building coral in the region. We tested the hypothesis that coral bleaching resistance enhances reproductive capacity and offspring performance by examining the reproductive biology of colonies that bleached and recovered (B) and colonies that did not bleach (NB) in 2015 in the subsequent spawning seasons. The proportion of colonies that spawned was higher in 2016 than in 2017. Regardless of parental bleaching history, we found eggs with higher abnormality and bundles with fewer eggs in 2016 than 2017. While reproductive output was similar between B and NB colonies in 2016, survivorship of offspring that year were significantly influenced by the parental bleaching history (egg donor × sperm donor: B × B, B × NB, NB × B, and NB × NB). Offspring produced by NB egg donors had the highest survivorship, while offspring from previously bleached colonies had the lowest survivorship, highlighting the negative effects of bleaching on parental investment and offspring performance. While sexual reproduction continues inM.capitatapost-bleaching, gametes are differentially impacted by recovery time following a bleaching event and by parental bleaching resistance. Our results demonstrate the importance of identifying bleaching resistant individuals during and after heating events. This study further highlights the significance of maternal effects through potential egg provisioning for offspring survivorship and provides a baseline for human-assisted intervention (i.e., selective breeding) to mitigate the effects of climate change on coral reefs. 

In mesophotic coral ecosystems, reef-building corals and their photosynthetic symbionts can survive with less than 1% of surface irradiance. How depth-specialist corals rely upon autotrophically and heterotrophically derived energy sources across the mesophotic zone remains unclear. We analysed the stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope values of aLeptoseriscommunity from the ‘Au‘au Channel, Maui, Hawai‘i (65–125 m) including four coral host species living symbiotically with three algal haplotypes. We characterized the isotope values of hosts and symbionts across species and depth to compare trophic strategies. Symbiontδ¹³C was consistently 0.5‰ higher than hostδ¹³C at all depths. Mean colony host and symbiontδ¹⁵N differed by up to 3.7‰ at shallow depths and converged at deeper depths. These results suggest that both heterotrophy and autotrophy remained integral to colony survival across depth. The increasing similarity between host and symbiontδ¹⁵N at deeper depths suggests that nitrogen is more efficiently shared between mesophotic coral hosts and their algal symbionts to sustain autotrophy. Isotopic trends across depth did not generally vary by host species or algal haplotype, suggesting that photosynthesis remains essential toLeptoserissurvival and growth despite low light availability in the mesophotic zone. 

The persistence of coral reefs requires the survival of adult coral colonies and their continued sexual reproduction despite thermal stress. To assess the trophic pathway (i.e., autotrophy and/or heterotrophy) used to develop gametes following bleaching, we thermally stressedMontipora capitatafor one month at a time when corals in Hawai’i typically experience elevated seawater temperatures. After six and nine months of recovery, we pulse-chased non-bleached and previously bleached colonies using a dual-label design to compare the allocation of carbon and nitrogen at significant stages of gamete development. Dissolved inorganic carbon- (DI¹³C) and nitrogen- (DI¹⁵N) labelled seawater or¹³C- and¹⁵N-labelled rotifers were used to assess the autotrophic and heterotrophic pathways, respectively. At multiple time points for up to two years later, we collected adult coral fragments and isolated host tissue, Symbiodiniaceae cells, and developing eggs and captured gamete bundles to analyze their carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotopes. We found that the presence of Symbiodiniaceae was important for gametogenesis in both non-bleached and previously bleached colonies in two main ways. First, autotrophically-acquired carbon and nitrogen were both allocated to gametes during development, suggesting that recovery of photosynthesis after bleaching is critical for gametogenesis. Second, only heterotrophically-acquired nitrogen, not carbon, was incorporated into gametes and was readily recycled between host tissues and Symbiodiniaceae cells. This suggests that one of the purposes of heterotrophy following coral bleaching forM. capitatamay be to supplement the nitrogen pool, providing available nutrients for endosymbiotic algal growth. Allocation of carbon and nitrogen to eggs coincided with the period when vertical transmission of symbionts to gametes occurs, further supporting the important relationship between gametogenesis and availability of Symbiodiniaceae forM. capitata.