Common types of microdebris affect the physiology of reef-building corals.

Marine debris, particularly microdebris (< 1 mm) poses a potential threat to marine life, including reef-building corals. While previous research has mainly focused on the impact of single polymer microplastics, the effects of natural microdebris, composed of a mixture of materials, have not been explored. Therefore, this study aimed to assess the effects of different microdebris, originating from major sources of pollution, on reef-building corals. For this, we exposed two scleractinian coral species, Pocillopora verrucosa and Stylophora pistillata, known to frequently ingest microplastics, to four types of microdebris in an 8-week laboratory experiment: fragmented environmental plastic debris, artificial fibers from clothing, residues from the automobile sector consisting of tire wear, brake abrasion, and varnish flakes, a single polymer microplastic treatment consisting of polyethylene particles, and a microdebris-free control treatment. Specifically, we (I) compared the effects of the different microdebris on coral growth, necrosis, and photosynthesis, (II) investigated the difference between the microdebris mixtures and the exposure to the single polymer treatment, and (III) identified potential mechanisms causing species-specific effects by contrasting the feeding responses of the two coral species on microdebris and natural food. We show that the fibers and tire wear had the strongest effects on coral physiology, with P. verrucosa being more affected than S. pistillata. Both species showed increased volume growth in response to the microdebris treatments, accompanied by decreased calcification in P. verrucosa. Photosynthetic efficiency of the symbionts was enhanced in both species. The species-specific physiological responses might be attributed to feeding reactions, with P. verrucosa responding significantly more often to microdebris than S. pistillata. These findings highlight the effect of different microdebris on coral physiology and the need for future studies to use particle mixtures to better mimic naturally occurring microdebris and assess its effect on corals in more detail.

Feeding responses of reef-building corals provide species- and concentration-dependent risk assessment of microplastic.

The negative impacts of microplastic on reef-building corals are often attributed to the feeding responses to these particles. Although reactions to and ingestion of microplastic are frequently reported, a quantitative comparison to natural particles and of the factors influencing these responses is largely missing. Thus, this study aims to compare the feeding rates of corals to microplastic and natural particles, considering factors influencing these responses. Specifically, we I) studied the feeding responses of corals to microplastic, natural food, and non-food particles, II) examined the influence of biotic factors (i.e., biofilm on the particles and presence of natural food), III) evaluated species-specific differences in feeding responses to microplastic particles, and IV) applied a toxicodynamic model for species- and concentration-dependent risk assessments. We assessed the feeding responses of 11 coral species, spanning different life-history strategies and growth forms in experimental feeding trials. The results showed that the feeding responses of corals to microplastic differ from those to naturally occurring particles. Reactions to microplastic and natural food occurred equally often, while sand was more frequently rejected. Yet, the ingestion process was much more selective, and microplastic was ingested less frequently than natural food. The presence of a biofilm and natural food had activating effects on the feeding behavior of the corals on microplastic. Generally, coral species that exhibit a higher degree of heterotrophic feeding also reacted more often to microplastic. The species- and concentration-dependent toxicodynamic risk model built on these data reveals that most tested coral species are unlikely to be at risk under present environmental concentration levels. However, highly heterotrophic feeders, such as Blastomussa merleti, or generally vulnerable species, such as Pocillopora verrucosa, need special consideration. These findings help to better evaluate the responses of corals to microplastic and their risk in an increasingly polluted ocean.

Horizon scanning the application of probiotics for wildlife.

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.

Diversity of the Pacific Ocean coral reef microbiome.

Coral reefs are among the most diverse ecosystems on Earth. They support high biodiversity of multicellular organisms that strongly rely on associated microorganisms for health and nutrition. However, the extent of the coral reef microbiome diversity and its distribution at the oceanic basin-scale remains to be explored. Here, we systematically sampled 3 coral morphotypes, 2 fish species, and planktonic communities in 99 reefs from 32 islands across the Pacific Ocean, to assess reef microbiome composition and biogeography. We show a very large richness of reef microorganisms compared to other environments, which extrapolated to all fishes and corals of the Pacific, approximates the current estimated total prokaryotic diversity for the entire Earth. Microbial communities vary among and within the 3 animal biomes (coral, fish, plankton), and geographically. For corals, the cross-ocean patterns of diversity are different from those known for other multicellular organisms. Within each coral morphotype, community composition is always determined by geographic distance first, both at the island and across ocean scale, and then by environment. Our unprecedented sampling effort of coral reef microbiomes, as part of the Tara Pacific expedition, provides new insight into the global microbial diversity, the factors driving their distribution, and the biocomplexity of reef ecosystems.

Ecology of Endozoicomonadaceae in three coral genera across the Pacific Ocean.

Health and resilience of the coral holobiont depend on diverse bacterial communities often dominated by key marine symbionts of the Endozoicomonadaceae family. The factors controlling their distribution and their functional diversity remain, however, poorly known. Here, we study the ecology of Endozoicomonadaceae at an ocean basin-scale by sampling specimens from three coral genera (Pocillopora, Porites, Millepora) on 99 reefs from 32 islands across the Pacific Ocean. The analysis of 2447 metabarcoding and 270 metagenomic samples reveals that each coral genus harbored a distinct new species of Endozoicomonadaceae. These species are composed of nine lineages that have distinct biogeographic patterns. The most common one, found in Pocillopora, appears to be a globally distributed symbiont with distinct metabolic capabilities, including the synthesis of amino acids and vitamins not produced by the host. The other lineages are structured partly by the host genetic lineage in Pocillopora and mainly by the geographic location in Porites. Millepora is more rarely associated to Endozoicomonadaceae. Our results show that different coral genera exhibit distinct strategies of host-Endozoicomonadaceae associations that are defined at the bacteria lineage level.

Integrative omics framework for characterization of coral reef ecosystems from the Tara Pacific expedition.

Coral reef science is a fast-growing field propelled by the need to better understand coral health and resilience to devise strategies to slow reef loss resulting from environmental stresses. Key to coral resilience are the symbiotic interactions established within a complex holobiont, i.e. the multipartite assemblages comprising the coral host organism, endosymbiotic dinoflagellates, bacteria, archaea, fungi, and viruses. Tara Pacific is an ambitious project built upon the experience of previous Tara Oceans expeditions, and leveraging state-of-the-art sequencing technologies and analyses to dissect the biodiversity and biocomplexity of the coral holobiont screened across most archipelagos spread throughout the entire Pacific Ocean. Here we detail the Tara Pacific workflow for multi-omics data generation, from sample handling to nucleotide sequence data generation and deposition. This unique multidimensional framework also includes a large amount of concomitant metadata collected side-by-side that provide new assessments of coral reef biodiversity including micro-biodiversity and shape future investigations of coral reef dynamics and their fate in the Anthropocene.

Frenemies on the reef? Resolving the coral-Endozoicomonas association.

Stony corals are poster child holobionts due to their intimate association with diverse microorganisms from all domains of life. We are only beginning to understand the diverse functions of most of these microbial associates, including potential main contributors to holobiont health and resilience. Among these, bacteria of the elusive genus Endozoicomonas are widely perceived as beneficial symbionts based on their genomic potential and their high prevalence and ubiquitous presence in coral tissues. Simultaneously, evidence of pathogenic and parasitic Endozoicomonas lineages in other marine animals is emerging. Synthesizing the current knowledge on the association of Endozoicomonas with marine holobionts, we challenge the perception of a purely mutualistic coral-Endozoicomonas relationship and propose directions to elucidate its role along the symbiotic spectrum.

Harnessing the Power of Model Organisms To Unravel Microbial Functions in the Coral Holobiont.

Stony corals build the framework of coral reefs, ecosystems of immense ecological and economic importance. The existence of these ecosystems is threatened by climate change and other anthropogenic stressors that manifest in microbial dysbiosis such as coral bleaching and disease, often leading to coral mortality. Despite a significant amount of research, the mechanisms ultimately underlying these destructive phenomena, and what could prevent or mitigate them, remain to be resolved. This is mostly due to practical challenges in experimentation on corals and the highly complex nature of the coral holobiont that also includes bacteria, archaea, protists, and viruses. While the overall importance of these partners is well recognized, their specific contributions to holobiont functioning and their interspecific dynamics remain largely unexplored. Here, we review the potential of adopting model organisms as more tractable systems to address these knowledge gaps. We draw on parallels from the broader biological and biomedical fields to guide the establishment, implementation, and integration of new and emerging model organisms with the aim of addressing the specific needs of coral research. We evaluate the cnidarian models Hydra, Aiptasia, Cassiopea, and Astrangia poculata; review the fast-evolving field of coral tissue and cell cultures; and propose a framework for the establishment of "true" tropical reef-building coral models. Based on this assessment, we also suggest future research to address key aspects limiting our ability to understand and hence improve the response of reef-building corals to future ocean conditions.

Reef-building corals act as long-term sink for microplastic.

The pollution of the marine environment with microplastics is pervasive. However, microplastic concentrations in the seawater are lower than the number of particles entering the oceans, suggesting that plastic particles accumulate in environmental sinks. Yet, the exact long-term sinks related to the "missing plastic" phenomenon are barely explored. Sediments in nearshore biogenic habitats are known to trap large amounts of microplastics, but also the three-dimensional structures of coral reefs might serve as unique, living long-term sinks. The main framework builders, reef-building corals, have been shown to ingest and overgrow microplastics, potentially leading to a deposition of particles in reef structures. However, little is known about the number of deposited particles and the underlying processes determining the permanent deposition in the coral skeletons. To test whether corals may act as living long-term sink for microplastic, we exposed four reef-building coral species to polyethylene microplastics (200 particles L-1 ) in an 18-month laboratory experiment. We found microplastics in all treatment specimens, with low numbers of particles trapped in the coral tissue (up to 2 particles per cm2 ) and much higher numbers in the skeleton (up to 84 particles per cm3 ). The numbers of particles accumulated in the coral skeletons were mainly related to coral growth (i.e., skeletal growth in volume), suggesting that deposition is a regularly occurring stochastic process. We estimate that reef-building corals may remove 0.09%-2.82% of the bioavailable microplastics from tropical shallow-reef waters per year. Our study shows for the first time that microplastic particles accumulate permanently in a biological sink, helping to explain the "missing plastic" phenomenon. This highlights the importance of coral reefs for the ecological balance of the oceans and reinforces the need to protect them, not only to mitigate the effects of climate change but also to preserve their ecosystem services as long-term sink for microplastic.

Projecting coral responses to intensifying marine heatwaves under ocean acidification.

Over this century, coral reefs will run the gauntlet of climate change, as marine heatwaves (MHWs) become more intense and frequent, and ocean acidification (OA) progresses. However, we still lack a quantitative assessment of how, and to what degree, OA will moderate the responses of corals to MHWs as they intensify throughout this century. Here, we first projected future MHW intensities for tropical regions under three future greenhouse gas emissions scenario (representative concentration pathways, RCP2.6, RCP4.5 and RCP8.5) for the near-term (2021-2040), mid-century (2041-2060) and late-century (2081-2100). We then combined these MHW intensity projections with a global data set of 1,788 experiments to assess coral attribute performance and survival under the three emissions scenarios for the near-term, mid-century and late-century in the presence and absence of OA. Although warming and OA had predominately additive impacts on the coral responses, the contribution of OA in affecting most coral attributes was minor relative to the dominant role of intensifying MHWs. However, the addition of OA led to greater decreases in photosynthesis and survival under intermediate and unrestricted emissions scenario for the mid- and late-century than if intensifying MHWs were considered as the only driver. These results show that role of OA in modulating coral responses to intensifying MHWs depended on the focal coral attribute and extremity of the scenario examined. Specifically, intensifying MHWs and OA will cause increasing instances of coral bleaching and substantial declines in coral productivity, calcification and survival within the next two decades under the low and intermediate emissions scenario. These projections suggest that corals must rapidly adapt or acclimatize to projected ocean conditions to persist, which is far more likely under a low emissions scenario and with increasing efforts to manage reefs to enhance resilience.

Effects of Ocean Acidification on Resident and Active Microbial Communities of Stylophora pistillata.

Ocean warming and ocean acidification (OA) are direct consequences of climate change and affect coral reefs worldwide. While the effect of ocean warming manifests itself in increased frequency and severity of coral bleaching, the effects of ocean acidification on corals are less clear. In particular, long-term effects of OA on the bacterial communities associated with corals are largely unknown. In this study, we investigated the effects of ocean acidification on the resident and active microbiome of long-term aquaria-maintained Stylophora pistillata colonies by assessing 16S rRNA gene diversity on the DNA (resident community) and RNA level (active community). Coral colony fragments of S. pistillata were kept in aquaria for 2 years at four different pCO2 levels ranging from current pH conditions to increased acidification scenarios (i.e., pH 7.2, 7.4, 7.8, and 8). We identified 154 bacterial families encompassing 2,047 taxa (OTUs) in the resident and 89 bacterial families including 1,659 OTUs in the active communities. Resident communities were dominated by members of Alteromonadaceae, Flavobacteriaceae, and Colwelliaceae, while active communities were dominated by families Cyclobacteriacea and Amoebophilaceae. Besides the overall differences between resident and active community composition, significant differences were seen between the control (pH 8) and the two lower pH treatments (7.2 and 7.4) in the active community, but only between pH 8 and 7.2 in the resident community. Our analyses revealed profound differences between the resident and active microbial communities, and we found that OA exerted stronger effects on the active community. Further, our results suggest that rDNA- and rRNA-based sequencing should be considered complementary tools to investigate the effects of environmental change on microbial assemblage structure and activity.

Interactive effects of microplastic pollution and heat stress on reef-building corals.

Plastic pollution is an emerging stressor that increases pressure on ecosystems such as coral reefs that are already challenged by climate change. However, the effects of plastic pollution in combination with global warming are largely unknown. Thus, the goal of this study was to determine the cumulative effects of microplastic pollution with that of global warming on reef-building coral species and to compare the severity of both stressors. For this, we conducted a series of three controlled laboratory experiments and exposed a broad range of coral species (Acropora muricata, Montipora digitata, Porites lutea, Pocillopora verrucosa, and Stylophora pistillata) to microplastic particles in a range of concentrations (2.5-2500 particles L-1) and mixtures (from different industrial sectors) at ambient temperatures and in combination with heat stress. We show that microplastic can occasionally have both aggravating or mitigating effects on the corals' thermal tolerance. In comparison to heat stress, however, microplastic constitutes a minor stressor. While heat stress led to decreased photosynthetic efficiency of algal symbionts, and increased bleaching, tissue necrosis, and mortality, treatment with microplastic particles had only minor effects on the physiology and health of the tested coral species at ambient temperatures. These findings underline that while efforts to reduce plastic pollution should continue, they should not replace more urgent efforts to halt global warming, which are immediately needed to preserve remaining coral reef ecosystems.

Integrating environmental variability to broaden the research on coral responses to future ocean conditions.

Our understanding of the response of reef-building corals to changes in their physical environment is largely based on laboratory experiments, analysis of long-term field data, and model projections. Experimental data provide unique insights into how organisms respond to variation of environmental drivers. However, an assessment of how well experimental conditions cover the breadth of environmental conditions and variability where corals live successfully is missing. Here, we compiled and analyzed a globally distributed dataset of in-situ seasonal and diurnal variability of key environmental drivers (temperature, pCO2 , and O2 ) critical for the growth and livelihood of reef-building corals. Using a meta-analysis approach, we compared the variability of environmental conditions assayed in coral experimental studies to current and projected conditions in their natural habitats. We found that annual temperature profiles projected for the end of the 21st century were characterized by distributional shifts in temperatures with warmer winters and longer warm periods in the summer, not just peak temperatures. Furthermore, short-term hourly fluctuations of temperature and pCO2 may regularly expose corals to conditions beyond the projected average increases for the end of the 21st century. Coral reef sites varied in the degree of coupling between temperature, pCO2 , and dissolved O2 , which warrants site-specific, differentiated experimental approaches depending on the local hydrography and influence of biological processes on the carbonate system and O2 availability. Our analysis highlights that a large portion of the natural environmental variability at short and long timescales is underexplored in experimental designs, which may provide a path to extend our understanding on the response of corals to global climate change.

A comparative baseline of coral disease in three regions along the Saudi Arabian coast of the central Red Sea.

Coral disease is a growing problem for coral reefs globally and diseases have been linked to thermal stress, excess nutrients, overfishing and other human impacts. The Red Sea is a unique environment for corals with a strong environmental gradient characterized by temperature extremes and high salinities, but minimal terrestrial runoff or riverine input and their associated pollution. Yet, relatively little is known about coral diseases in this region. Disease surveys were conducted at 22 reefs within three regions (Yanbu, Thuwal, Al Lith) in the central Red Sea along the Saudi Arabian coast. Surveys occurred in October 2015, which coincided with a hyperthermal-induced bleaching event. Our objectives were to 1) document types, prevalence, and distribution of coral diseases in a region with minimal terrestrial input, 2) compare regional differences in diseases and bleaching along a latitudinal gradient of environmental conditions, and 3) use histopathology to characterize disease lesions at the cellular level. Coral reefs of the central Red Sea had a widespread but a surprisingly low prevalence of disease (<0.5%), based on the examination of >75,750 colonies. Twenty diseases were recorded affecting 16 coral taxa and included black band disease, white syndromes, endolithic hypermycosis, skeletal eroding band, growth anomalies and focal bleached patches. The three most common diseases were Acropora white syndrome (59.1% of the survey sites), Porites growth anomalies (40.9%), and Porites white syndrome (31.8%). Sixteen out of 30 coral genera within transects had lesions and Acropora, Millepora and Lobophyllia were the most commonly affected. Cell-associated microbial aggregates were found in four coral genera including a first report in Stylophora. Differences in disease prevalence, coral cover, amount of heat stress as measured by degree heating weeks (DHW) and extent of bleaching was evident among sites. Disease prevalence was not explained by coral cover or DHW, and a negative relationship between coral bleaching and disease prevalence was found. The northern-most sites off the coast of Yanbu had the highest average disease prevalence and highest average DHW values but no bleaching. Our study provides a foundation and baseline data for coral disease prevalence in the central Red Sea, which is projected to increase as a consequence of increased frequency and severity of ocean warming.

Insights into the Cultured Bacterial Fraction of Corals.

Bacteria associated with coral hosts are diverse and abundant, with recent studies suggesting involvement of these symbionts in host resilience to anthropogenic stress. Despite their putative importance, 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 bacteria isolated from corals originating from tropical, temperate, and cold-water habitats. A total of 3,055 isolates from 52 studies were considered by our metasurvey. Of these, 1,045 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 bacterium-coral symbioses among the strains. 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-bacterium symbioses-potentially involved in host colonization and host-symbiont recognition, antiviral defense 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 holistic and customized reef restoration and rehabilitation efforts. IMPORTANCE 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. This equated to 1,045 individual isolates which had full-length 16S rRNA gene sequences, after filtering of the original 3,055. We also explored which of these had genomes available. Originally, only 36 were available, and as part of this study, we added a further 38-equating to 74 in total. From this, we investigated potential genetic signatures that may facilitate a host-associated lifestyle. Further, such a resource is an important step in the selection of probiotic candidates, which are being investigated for promoting coral resilience and potentially applied as a novel strategy in reef restoration and rehabilitation efforts. In the spirit of open access, we have ensured this collection is available to the wider research community through the web site http://isolates.reefgenomics.org/ with the hope many scientists across the globe will ask for access to these cultures for future studies.

Rebuild the Academy: Supporting academic mothers during COVID-19 and beyond.

The issues facing academic mothers have been discussed for decades. Coronavirus Disease 2019 (COVID-19) is further exposing these inequalities as womxn scientists who are parenting while also engaging in a combination of academic related duties are falling behind. These inequities can be solved by investing strategically in solutions. Here we describe strategies that would ensure a more equitable academy for working mothers now and in the future. While the data are clear that mothers are being disproportionately impacted by COVID-19, many groups could benefit from these strategies. Rather than rebuilding what we once knew, let us be the architects of a new world.

Coral-Associated Viral Assemblages From the Central Red Sea Align With Host Species and Contribute to Holobiont Genetic Diversity.

Coral reefs are highly diverse marine ecosystems increasingly threatened on a global scale. The foundation species of reef ecosystems are stony corals that depend on their symbiotic microalgae and bacteria for aspects of their metabolism, immunity, and environmental adaptation. Conversely, the function of viruses in coral biology is less well understood, and we are missing an understanding of the diversity and function of coral viruses, particularly in understudied regions such as the Red Sea. Here we characterized coral-associated viruses using a large metagenomic and metatranscriptomic survey across 101 cnidarian samples from the central Red Sea. While DNA and RNA viral composition was different across coral hosts, biological traits such as coral life history strategy correlated with patterns of viral diversity. Coral holobionts were broadly associated with Mimiviridae and Phycodnaviridae that presumably infect protists and algal cells, respectively. Further, Myoviridae and Siphoviridae presumably target members of the bacterial phyla Actinobacteria, Firmicutes, and Proteobacteria, whereas Hepadnaviridae and Retroviridae might infect the coral host. Genes involved in bacterial virulence and auxiliary metabolic genes were common among the viral sequences, corroborating a contribution of viruses to the holobiont's genetic diversity. Our work provides a first insight into Red Sea coral DNA and RNA viral assemblages and reveals that viral diversity is consistent with global coral virome patterns.

Author Correction: Robustness to extinction and plasticity derived from mutualistic bipartite ecological networks.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

A framework for in situ molecular characterization of coral holobionts using nanopore sequencing.

Molecular characterization of the coral host and the microbial assemblages associated with it (referred to as the coral holobiont) is currently undertaken via marker gene sequencing. This requires bulky instruments and controlled laboratory conditions which are impractical for environmental experiments in remote areas. Recent advances in sequencing technologies now permit rapid sequencing in the field; however, development of specific protocols and pipelines for the effective processing of complex microbial systems are currently lacking. Here, we used a combination of 3 marker genes targeting the coral animal host, its symbiotic alga, and the associated bacterial microbiome to characterize 60 coral colonies collected and processed in situ, during the Tara Pacific expedition. We used Oxford Nanopore Technologies to sequence marker gene amplicons and developed bioinformatics pipelines to analyze nanopore reads on a laptop, obtaining results in less than 24 h. Reef scale network analysis of coral-associated bacteria reveals broadly distributed taxa, as well as host-specific associations. Protocols and tools used in this work may be applicable for rapid coral holobiont surveys, immediate adaptation of sampling strategy in the field, and to make informed and timely decisions in the context of the current challenges affecting coral reefs worldwide.