Large genome databases have markedly improved our understanding of marine microorganisms1-5. Although these resources have focused on prokaryotes, genomes from many dominant marine lineages, such as Pelagibacter and Prochlorococcus, are conspicuously underrepresented. Here we present the Great Barrier Reef Microbial Genomes Database (GBR-MGD), comprising 5,283 prokaryotic genomes obtained from Great Barrier Reef seawater samples using Nanopore and Illumina sequencing, including a collection of high-quality genomes of underrepresented groups. We show that standard short-read assemblies miss these populations owing to a combination of strain heterogeneity and low-GC-percentage sequencing bias. The GBR-MGD also comprises 20 chromosome-level picoeukaryote and 808,585 viral genomes, including a newly described clade of marine Crassvirales. We demonstrate the utility of the GBR-MGD to identify indicator taxa that can reliably predict the effects of reef management practices, such as the establishment of marine protected zones.

The stability of the symbiotic relationship between coral and their dinoflagellate algae (Symbiodiniaceae) is disrupted by ocean warming. Although the coral thermal response depends on the complex interactions between host, Symbiodiniaceae and prokaryotes, the mechanisms underlying the initial destabilization of these symbioses are poorly understood. In a 2-month manipulative experiment, we exposed the coral Porites lutea to gradually increasing temperatures corresponding to 0–8 degree heating weeks (DHW) and assessed the response of the coral holobiont using coral and Symbiodiniaceae transcriptomics, microbial 16S rRNA gene sequencing and physiological measurements. From early stages of heat stress (< 1 DHW), the increase in metabolic turnover shifted the holobiont to a net heterotrophic state in which algal-derived nutrients were insufficient to meet host energy demands, resulting in reduced holobiont performance at 1 DHW. We postulate the altered nutrient cycling also affected the coral-associated microbial community, with the relative abundance of Endozoicomonas bacteria declining under increasing heat stress. Integration of holobiont stress responses correlated this decline to an increase in expression of a host ADP-ribosylation factor, suggesting that Symbiodiniaceae and Endozoicomonas may underlie similar endosymbiotic regulatory processes. The thermotolerance of coral holobionts therefore is influenced by the nutritional status of its members and their interactions, and this identified metabolic interdependency highlights the importance of applying an integrative approach to guide coral reef conservation efforts.

BackgroundEvolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea.ResultsUsing a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the "Global Coral Microbiome Project") and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates.ConclusionsThese results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs.

>Dear Editor, Coral reefs sustain high biodiversity and have been referred to as the rainforests of the ocean. However, anthropogenic stressors have led to a global decline of coral reefs, partly due to the increasing scale, frequency, and intensity of coral bleaching events driven by global warming(Henley et al., 2024; Hughes et al., 2018).

Organismal communities associated with coral reefs, particularly invertebrates and microbes, play crucial roles in ecosystem maintenance and coral health. Here, we characterized the organismal composition of a healthy, non-urbanized reef (Site A) and a degraded, urbanized reef (Site B) in the Gulf of Eilat/Aqaba, Red Sea to assess its impact on coral health and physiology. Biomimetically designed terracotta tiles were conditioned for 6 months at both sites, then reciprocally transplanted, and scleractinian coral species, Acropora eurystoma and Stylophora pistillata, were attached for an additional 6 months. After 12 months, tiles from Site A transplanted to Site B exhibited greater invertebrate richness and diversity than Site B’s original tiles (via Cytochrome c. Oxidase subunit I metabarcoding). Key bacteria from the healthy reef were more prevalent on Site A tiles and on the tiles transplanted to Site B (via 16S rRNA gene sequencing). Corals originally from Site B attached to transplanted healthy tiles (Site A) showed higher photochemical capacity, increased endosymbionts, and reduced physiological stress, measured by total antioxidant capacity and an integrated biomarker response. Our findings demonstrate the successful transfer of organismal communities between reefs, highlighting the potential benefits of healthy reef-associated invertebrates and microbes on coral physiology and their implications for reef restoration strategies. Invertebrate and microbe communities support reef ecosystems and coral health. Here, the authors characterize these communities from degraded and healthy reefs, showing that transplanting these healthy communities improved coral health at degraded reefs.

Reef restoration activities and the ornamental trade are increasing the demand for sexually propagated corals. One challenge faced in scaling up the aquaculture production of corals is high mortality as a result of fouling organisms overgrowing coral spat, with manual removal of algae and other fouling organisms being costly and time consuming. Here we test the use of microherbivore grazers as a potential biocontrol method for fouling in coral aquaculture and compare their effectiveness to manual cleaning by an aquarist. Recruits of six coral species (Acropora millepora, Acropora kenti, Goniastrea retiformis, Porites lobata, Dipsastraea speciosa and Lobophyllia cor-ymbosa) were reared for 112 days with aquarist cleaning, or co-cultured with gastropods (Calthalotia strigata or Turbo haynesi), sea urchins (Tripneustes gratilla or Echinomentra mathaei), the hermit crab Clibanarius cf. taeniatus or under a control treatment with no grazers. Corals grown in the aquarist cleaning treatment displayed high survival and growth, though similar responses were observed for most coral species grown with C. strigata or T. gratilla, likely due to minimal damage via overgrazing and the promotion of relatively short turf algal com-munities in these treatments. However, effort required, measured as average cleaning time, was 2-3 times greater in the aquarist treatment compared to C. strigata or T. gratilla treatments. Survival of coral recruits housed with C. cf. taeniatus, E. mathaei or T. haynesi were variable, likely due to the dominance of long, filamentous turf algae in tanks with E. mathaei, and physical disturbance to recruits by C. cf. taeniatus and T. haynesi. Our results demonstrate microherbivores have potential for application in aquaculture to promote production, while also reducing labour costs.

Amphipod crustaceans exist across marine habitats from the polar regions to the tropics, providing a critical biological link between benthic/pelagic processes and marine/atmospheric ecosystems. They fulfil many functional roles as predators and prey, bioturbators, mesograzers, pollinators, secondary producers, nutrient cycling facilitators, and indicators of marine and sediment health. Despite their importance, tropical amphipods are poorly represented in the literature. This review offers an overview of the biological and ecological roles of amphipods globally. Amphipods face many pressures in the warming seas that will ultimately force acclimation, adaptation, or mortality, with potentially dire consequences for the processes they facilitate. We highlight the lack of data on tropical amphipods and argue an urgent need to identify their diversity, abundance, and functions underpinning resilience in ecosystems such as coral reefs, seagrass meadows, and mangroves. This improved understanding is necessary to predict and potentially mitigate cascading deleterious effects driven by a rapidly warming planet.

Biodegradation of microplastics facilitated by natural marine biofouling is a promising approach for ocean bioremediation. However, implementation requires a comprehensive understanding of how interactions between the marine microbiome and dominant microplastic debris types (e.g., polymer and additive combinations) can influence biofilm development and drive biodegradation. To investigate this, polystyrene (PS) and polyvinyl chloride (PVC) microplastics (< 200 µm in diameter) were prepared either without any additives (i.e., virgin) or containing 15 wt% of the plasticisers diethylhexyl phthalate (DEHP) or bisphenol A (BPA). Each polymer-plasticiser microplastic combination was exposed to environmentally relevant conditions in a simulated seawater mesocosm representative of tropical reef waters over a 21-day period to allow for natural biofilm development. Following this, microplastic degradation and the colonising bacterial biofilm was assessed as a function of time, polymer and plasticiser type using infrared, thermal, gel permeation and surface characterisation techniques, as well as 16S ribosomal RNA bacterial gene sequencing, respectively. Together, these analyses revealed time-, polymer- and plasticiser-dependent degradation, particularly of the PS-BPA microplastics. Degradation of the PS-BPA microplastics also coincided with changes in bacterial community composition and an increased total relative abundance of putative biodegradative bacteria. These findings indicate that the metabolic potential and biodegradative capability of the colonising marine biofilm can be significantly impacted by the chemical properties of the microplastic substrate, even within short timeframes.

Microbial diversity has been extensively explored in reef-building corals. However, the functional roles of coral-associated microorganisms remain poorly elucidated. Here, we recover 191 bacterial and 10 archaeal metagenome-assembled genomes (MAGs) from the coral Acropora kenti (formerly A. tenuis) and adjacent seawater, to identify microbial functions and metabolic interactions within the holobiont. We show that 82 MAGs were specific to the A. kenti holobiont, including members of the Pseudomonadota, Bacteroidota, and Desulfobacterota. A. kenti-specific MAGs displayed significant differences in their genomic features and functional potential relative to seawater-specific MAGs, with a higher prevalence of genes involved in host immune system evasion, nitrogen and carbon fixation, and synthesis of five essential B-vitamins. We find a diversity of A. kenti-specific MAGs encode the biosynthesis of essential amino acids, such as tryptophan, histidine, and lysine, which cannot be de novo synthesised by the host or Symbiodiniaceae. Across a water quality gradient spanning 2° of latitude, A. kenti microbial community composition is correlated to increased temperature and dissolved inorganic nitrogen, with corresponding enrichment in molecular chaperones, nitrate reductases, and a heat-shock protein. We reveal mechanisms of A. kenti-microbiome-symbiosis on the Great Barrier Reef, highlighting the interactions underpinning the health of this keystone holobiont.

Endosymbiotic dinoflagellates (Symbiodiniaceae) influence coral thermal tolerance at both local and regional scales. In isolation, the effects of host genetics, environment, and thermal disturbances on symbiont communities are well understood, yet their combined effects remain poorly resolved. Here, we investigate Symbiodiniaceae across 1300 km in Australia's Coral Sea Marine Park to disentangle these interactive effects. We identified Symbiodiniaceae to species-level resolution for three coral species ( Acropora cf humilis, Pocillopora verrucosa , and Pocillopora meandrina ) by sequencing two genetic markers of the symbiont (ITS2 and psbA ncr ), paired with genotype-by-sequencing of the coral host (DArT-seq). Our samples predominantly returned sequences from the genus Cladocopium , where Acropora cf humilis affiliated with C3k, Pocillopora verrucosa with C. pacificum , and Pocillopora meandrina with C. latusorum . Multivariate analyses revealed that Acropora symbionts were driven strongly by local environment and thermal disturbances. In contrast, Pocillopora symbiont communities were both partitioned 2.5-fold more by host genetic structure than by environmental structure. Among the two Pocillopora species, the effects of environment and host genetics explained four times more variation in symbionts for P. meandrina than P. verrucosa. The concurrent bleaching event in 2020 had variable impacts on symbiont communities, consistent with patterns in P. verrucosa and A. cf humilis , but not P. meandrina . Our findings demonstrate how symbiont macroscale community structure responses to environmental gradients depend on host species and their respective population structure. Integrating host, symbiont, and environmental data will help forecast the adaptive potential of corals and their symbionts amidst a rapidly changing environment.

Abstract Corals are associated with diverse and abundant bacterial communities, some members of which may promote host health through the exclusion of pathogens, increased environmental resilience, and by extending metabolic pathways in the holobiont. Much of our understanding of the microbiomes associated with anthozoans is derived from studying Scleractinia, though the Alcyonacea also harbour diverse microbial communities. This study examined the bacterial community associated with the alcyoniid Lobophytum pauciflorum, using 16S rRNA gene amplicon sequencing to document patterns between colonies and within the inner tissue, outer tissue and the mucus layer microhabitats. Tissue layers hosted similar bacterial communities, dominated by sequences affiliated with Endozoicomonadaceae, particularly the genus Parendozoicomonas. Sequences affiliated with Spirochaetaceae were also abundant in some colonies but were less evenly distributed among colonies. The bacterial community associated with the mucus layer was distinct from the tissue layers and its phylogenetic diversity was two-fold higher. The results from this study demonstrate that L. pauciflorum hosts a diverse bacterial community that is relatively stable at the colony level. Importantly, this study identifies the microhabitat specific communities that may have important roles in Alcyonacea health.

Abstract Background The positive effects of exposing corals to microorganisms have been reported though how the benefits are conferred are poorly understood. Here, we isolated an actinobacterial strain (SCSIO 13291) from Pocillopora damicornis with capabilities to synthesize antioxidants, vitamins, and antibacterial and antiviral compounds supported with phenotypic and/or genomic evidence. Strain SCSIO 13291 was labeled with 5 (and − 6)-carboxytetramethylrhodamine, succinimidyl ester and the labeled cell suspension directly inoculated onto the coral polyp tissues when nubbins were under thermal stress in a mesocosm experiment. We then visualized the labelled bacterial cells and analyzed the coral physiological, transcriptome and microbiome to elucidate the effect this strain conferred on the coral holobiont under thermal stress. Results Subsequent microscopic observations confirmed the presence of the bacterium attached to the coral polyps. Addition of the SCSIO 13291 strain reduced signs of bleaching in the corals subjected to heat stress. At the same time, alterations in gene expression, which were involved in reactive oxygen species and light damage mitigation, attenuated apoptosis and exocytosis in addition to metabolite utilization, were observed in the coral host and Symbiodiniaceae populations. In addition, the coral associated bacterial community altered with a more stable ecological network for samples inoculated with the bacterial strain. Conclusions Our results provide insights into the benefits of a putative actinobacterial probiotic strain that mitigate coral bleaching signs. This study suggests that the inoculation of bacteria can potentially directly benefit the coral holobiont through conferring metabolic activities or through indirect mechanisms of suppling additional nutrient sources.

Studies focused on understanding drivers of coral mortality often examine reef- or ecosystem-scale stressors and/or pulse events such as mass bleaching or disease outbreaks. While such work provides valuable information about large-scale changes to reef ecosystems, how stressors interact at the individual colony level across non-disturbance years is less understood. In this study, we tracked the fate of 400 plating Acropora coral colonies from 2 mid- and 2 outer-shelf reefs for 18 mo and examined (1) temporal changes in the prevalence of stressors, (2) how stressors affected the survival of individual colonies, and (3) survival rates of colonies after contracting disease. We found that 35.5% of all colonies died within the 18 mo observation period, a period free from acute disturbances (e.g. cyclones, mass bleaching, crown-of-thorns starfish [CoTS] outbreaks). Despite its low prevalence, predation (by Drupella spp. or CoTS) led to the greatest risk of complete mortality compared to corals that experienced no stressors (over 10-fold increased risk). Similarly, experiencing disease and physical injury (fragmentation, dislodgement) also increased the risk of complete mortality (~4-fold and ~2-fold, respectively). In contrast, while compromised health (i.e. bleaching, algal overgrowth) was common, this did not significantly increase the risk of colony mortality. Survival analysis of colonies with white syndrome showed that colonies exposed to stressors prior to contracting disease were 3 times more likely to die compared to colonies with disease alone. Our results highlight the complex interactions that occur among multiple stressors on coral reefs, even in non-disturbance years, and quantify the increased risk of mortality for colonies experiencing accumulated stressors.

Microbes play a critical role in the development and health of marine invertebrates, though microbial dynamics across life stages and host generations remain poorly understood in most reef species, especially in the context of climate change. Here, we use a 4-year multigenerational experiment to explore microbe-host interactions under the Intergovernmental Panel on Climate Change (IPCC)-forecast climate scenarios in the rock-boring tropical urchin Echinometra sp. A. Adult urchins (F0) were exposed for 18 months to increased temperature and pCO2 levels predicted for years 2050 and 2100 under RCP 8.5, a period which encompassed spawning. After rearing F1 offspring for a further 2 years, spawning was induced, and F2 larvae were raised under current day and 2100 conditions. Cross-generational climate effects were also explored in the microbiome of F1 offspring through a transplant experiment. Using 16S rRNA gene sequence analysis, we determined that each life stage and generation was associated with a distinct microbiome, with higher microbial diversity observed in juveniles compared to larval stages. Although life-stage specificity was conserved under climate conditions projected for 2050 and 2100, we observed changes in the urchin microbial community structure within life stages. Furthermore, we detected a climate-mediated parental effect when juveniles were transplanted among climate treatments, with the parental climate treatment influencing the offspring microbiome. Our findings reveal a potential for cross-generational impacts of climate change on the microbiome of a tropical invertebrate species.

Macroalgae removal is a proposed management option in the GBR to reverse declines in inshore coral reef health. Automated image analysis (AIA) is a valuable tool to assess benthic community assemblages. This study compared the accuracy of benthic community assemblages assessed through the AIA program CoralNet to manual image analysis. The ecological effect of macroalgae removal on benthic community composition was also investigated on established permanent quadrats (5x5 m) for reefs at Florence and Arthur Bay, Magnetic Island. Control and treatment quadrats (n=3 respectively) were photographed before and after macroalgae removal over 6 months. The results obtained by AIA and manual approaches were consistent, with macroalgae cover is approximately 77%-87% in all quadrats before macroalgal removal. Through the monitoring period, a small increase in coral cover in the macroalgal removal quadrats was observed in Florence and Arthur Bay (an increase of 1.8% and 0.1%, respectively). CoralNet was demonstrated to be robust for assessing reef benthic cover with no significant difference in recorded benthic categories when compared to the manual approach. CoralNet was accurate for identifying broad benthic categories, but less effective than manual image analyses for lower taxonomic categories (i.e., genus or species level).

Scleractinian coral populations are increasingly exposed to conditions above their upper thermal limits due to marine heatwaves, contributing to global declines of coral reef ecosystem health. However, historic mass bleaching events indicate there is considerable inter‐ and intra‐specific variation in thermal tolerance whereby species, individual coral colonies and populations show differential susceptibility to exposure to elevated temperatures. Despite this, we lack a clear understanding of how heat tolerance varies across large contemporary and historical environmental gradients, or the selective pressures that underpin this variation. Here we conducted standardised acute heat stress experiments to identify variation in heat tolerance among species and isolated reefs spanning a large environmental gradient across the Coral Sea Marine Park. We quantified the photochemical yield (Fv/Fm) of coral samples in three coral species, Acropora cf humilis, Pocillopora meandrina, and Pocillopora verrucosa, following exposure to four temperature treatments (local ambient temperatures, and + 3°C, +6°C and + 9°C above local maximum monthly mean). We quantified the temperature at which Fv/Fm decreased by 50% (termed ED50) and used derived values to directly compare acute heat tolerance across reefs and species. The ED50 for Acropora was 0.4–0.7°C lower than either Pocillopora species, with a 0.3°C difference between the two Pocillopora species. We also recorded 0.9°C to 1.9°C phenotypic variation in heat tolerance among reefs within species, indicating spatial heterogeneity in heat tolerance across broad environmental gradients. Acute heat tolerance had a strong positive relationship to mild heatwave exposure over the past 35 years (since 1986) but was negatively related to recent severe heatwaves (2016–2020). Phenotypic variation associated with mild thermal history in local environments provides supportive evidence that marine heatwaves are selecting for tolerant individuals and populations; however, this adaptive potential may be compromised by the exposure to recent severe heatwaves.

The provision of probiotics benefits the health of a wide range of organisms, from humans to animals and plants. Probiotics can enhance stress resilience of endangered organisms, many of which are critically threatened by anthropogenic impacts. The use of so-called 'probiotics for wildlife' is a nascent application, and the field needs to reflect on standards for its development, testing, validation, risk assessment, and deployment. Here, we identify the main challenges of this emerging intervention and provide a roadmap to validate the effectiveness of wildlife probiotics. We cover the essential use of inert negative controls in trials and the investigation of the probiotic mechanisms of action. We also suggest alternative microbial therapies that could be tested in parallel with the probiotic application. Our recommendations align approaches used for humans, aquaculture, and plants to the emerging concept and use of probiotics for wildlife.

Algal turfs trap and retain particulates, however, little is known about the relationship between particulate accumulation and taxonomic composition of algal turfs. We investigated how particulate mass related to algal turf structure (length and density) and community composition (taxonomic and functional) on two disparate reefs. Particulate mass was positively related to algal turf length. By contrast, the relationship between particulate mass and turf density was more complex and followed a negative parabolic shape; density increased with particulate mass before stabilising and then declining. Community analyses showed taxonomic, but not functional group compositions differed significantly between reefs and with increasing particulate mass. Our results suggest high loads of particulates accumulated in algal turfs are related to a longer, lower density turf structure, typified by filamentous forms such as Cladophora. Changes in algal turf structure and composition could have a variety of bottom-up influences on coral reef ecosystems.

Bacteria commonly form aggregates in a range of coral species [termed coral-associated microbial aggregates (CAMAs)], although these structures remain poorly characterized despite extensive efforts studying the coral microbiome. Here, we comprehensively characterize CAMAs associated with Stylophora pistillata and quantify their cell abundance. Our analysis reveals that multiple Endozoicomonas phylotypes coexist inside a single CAMA. Nanoscale secondary ion mass spectrometry imaging revealed that the Endozoicomonas cells were enriched with phosphorus, with the elemental compositions of CAMAs different from coral tissues and endosymbiotic Symbiodiniaceae, highlighting a role in sequestering and cycling phosphate between coral holobiont partners. Consensus metagenome-assembled genomes of the two dominant Endozoicomonas phylotypes confirmed their metabolic potential for polyphosphate accumulation along with genomic signatures including type VI secretion systems allowing host association. Our findings provide unprecedented insights into Endozoicomonas-dominated CAMAs and the first direct physiological and genomic linked evidence of their biological role in the coral holobiont.