Description: The significance of bacteria for eukaryotic functioning is increasingly recognized. Coral reef ecosystems critically rely on the relationship between coral hosts and their intracellular photosynthetic dinoflagellates, but the role of the associated bacteria remains largely theoretical. Here, we set out to relate coral-associated bacterial communities of the fungid host species Ctenactis echinata to environmental settings (geographic location, substrate cover, summer/winter, nutrient and suspended matter concentrations) and coral host abundance. We show that bacterial diversity of C.echinata aligns with ecological differences between sites and that coral colonies sampled at the species' preferred habitats are primarily structured by one bacterial taxon (genus Endozoicomonas) representing more than 60% of all bacteria. In contrast, host microbiomes from lower populated coral habitats are less structured and more diverse. Our study demonstrates that the content and structure of the coral microbiome aligns with environmental differences and denotes habitat adequacy. Availability of a range of coral host habitats might be important for the conservation of distinct microbiome structures and diversity.

Description: Background: Sponges (Porifera) harbor distinct microbial consortia within their mesohyl interior. We herein analysed the hologenomes of Stylissa carteri and Xestospongia testudinaria, which notably differ in their microbiome content. Results: Our analysis revealed that S. carteri has an expanded repertoire of immunological domains, specifically Scavenger Receptor Cysteine-Rich (SRCR) like domains, compared to X. testudinaria. On the microbial side, metatranscriptome analyses revealed an overrepresentation of potential symbiosis-related domains in X. testudinaria. Conclusions: Our findings provide genomic insights into the molecular mechanisms underlying host-symbiont coevolution and may serve as a roadmap for future hologenome analyses.

Description: White Plague Disease (WPD) is implicated in coral reef decline in the Caribbean and is characterized by microbial community shifts in coral mucus and tissue. Studies thus far have focused on assessing microbial communities or the identification of specific pathogens, yet few have addressed holobiont response across metaorganism compartments in coral disease. Here, we report on the first metatranscriptomic assessment of the coral host, algal symbiont, and microbial compartment in order to survey holobiont structure and function in healthy and diseased samples from Orbicella faveolata collected at reef sites off Puerto Rico. Our data indicate holobiont-wide as well as compartment-specific responses to WPD. Gene expression changes in the diseased coral host involved proteins playing a role in innate immunity, cytoskeletal integrity, cell adhesion, oxidative stress, chemical defense, and retroelements. In contrast, the algal symbiont showed comparatively few expression changes, but of large magnitude, of genes related to stress, photosynthesis, and metal transport. Concordant with the coral host response, the bacterial compartment showed increased abundance of heat shock proteins, genes related to oxidative stress, DNA repair, and potential retroelement activity. Importantly, analysis of the expressed bacterial gene functions establishes the participation of multiple bacterial families in WPD pathogenesis and also suggests a possible involvement of viruses and/or phages in structuring the bacterial assemblage. In this study, we implement an experimental approach to partition the coral holobiont and resolve compartment- and taxa-specific responses in order to understand metaorganism function in coral disease.

Description: Sponges are important components of marine benthic environments and are associated with microbial symbionts that carry out ecologically relevant functions. Stylissa carteri is an abundant, low-microbial abundance species in the Red Sea. We aimed to achieve the functional and taxonomic characterization of the most actively expressed prokaryotic genes in S. carteri. Prokaryotic mRNA was enriched from sponge total RNA, sequenced using Illumina HiSeq technology and annotated using the metagenomics Rapid Annotation using Subsystem Technology (MG-RAST) pipeline. We detected high expression of archaeal ammonia oxidation and photosynthetic carbon fixation by members of the genus Synechococcus. Functions related to stress response and membrane transporters were among the most highly expressed by S. carteri symbionts. Unexpectedly, gene functions related to methylotrophy were highly expressed by gammaproteobacterial symbionts. The presence of seawater-derived microbes is indicated by the phylogenetic proximity of organic carbon transporters to orthologues of members from the SAR11 clade. In summary, we revealed the most expressed functions of the S. carteri-associated microbial community and linked them to the dominant taxonomic members of the microbiome. This work demonstrates the applicability of metatranscriptomics to explore poorly characterized symbiotic consortia and expands our knowledge of the ecologically relevant functions carried out by coral reef sponge symbionts.

Description: Coral reefs in the Red Sea belong to the most diverse and productive reef ecosystems worldwide, although they are exposed to strong seasonal variability, high temperature, and high salinity. These factors are considered stressful for coral reef biota and challenge reef growth in other oceans, but coral reefs in the Red Sea thrive despite these challenges. In the central Red Sea high temperatures, high salinities, and low dissolved oxygen on the one hand reflect conditions that are predicted for ‘future oceans’ under global warming. On the other hand, alkalinity and other carbonate chemistry parameters are considered favourable for coral growth. In coral reefs of the central Red Sea, temperature and salinity follow a seasonal cycle, while chlorophyll and inorganic nutrients mostly vary spatially, and dissolved oxygen and pH fluctuate on the scale of hours to days. Within these strong environmental gradients micro- and macroscopic reef communities are dynamic and demonstrate plasticity and acclimatisation potential. Epilithic biofilm communities of bacteria and algae, crucial for the recruitment of reef-builders, undergo seasonal community shifts that are mainly driven by changes in temperature, salinity, and dissolved oxygen. These variables are predicted to change with the progression of global environmental change and suggest an immediate effect of climate change on the microbial community composition of biofilms. Corals are so-called holobionts and associate with a variety of microbial organisms that fulfill important functions in coral health and productivity. For instance, coral-associated bacterial communities are more specific and less diverse than those of marine biofilms, and in many coral species in the central Red Sea they are dominated by bacteria from the genus Endozoicomonas. Generally, coral microbiomes align with ecological differences between reef sites. They are similar at sites where these corals are abundant and successful. Coral microbiomes reveal a measurable footprint of anthropogenic influence at polluted sites. Coral-associated communities of endosymbiotic dinoflagellates in central Red Sea corals are dominated by Symbiodinium from clade C. Some corals harbour the same specific symbiont with a high physiological plasticity throughout their distribution range, while others maintain a more flexible association with varying symbionts of high physiological specificity over depths, seasons, or reef locations. The coral-Symbiodinium endosymbiosis drives calcification of the coral skeleton, which is a key process that provides maintenance and formation of the reef framework. Calcification rates and reef growth are not higher than in other coral reef regions, despite the beneficial carbonate chemistry in the central Red Sea. This may be related to the comparatively high temperatures, as indicated by reduced summer calcification and long-term slowing of growth rates that correlate with ocean warming trends. Indeed, thermal limits of abundant coral species in the central Red Sea may have been exceeded, as evidenced by repeated mass bleaching events during previous years. Recent comprehensive baseline data from central Red Sea reefs allow for insight into coral reef functioning and for quantification of the impacts of environmental change in the region.

Description: Experts release a roadmap for harnessing the potential of assisted evolution to help save corals. The IPCC predicts that if warming reaches 2°C, 99% of all coral reefs will be lost in less than 30 years. It is clear that to ensure the future of corals, the highest priority must be reducing global greenhouse gas emissions. However, even with swift and substantial reductions in emissions, corals will continue to face increasing temperatures for the foreseeable future, which can result in extensive coral mortality and local extinction of some coral species. While recent studies have shown that corals may exhibit some degree of adaptation to ocean warming, it is unclear whether corals are able to survive the rate of temperature change during heat waves that will become more frequent under several climate change scenarios. If corals lack what it takes to naturally rapidly adapt to new environmental regimes, they may fail to survive a warming ocean. This is where assisted evolution could be a game-changer. Growing our understanding of the power of adaptation In January 2023, we held a workshop on assisted evolution co-organized with the Australian Institute of Marine Sciences (AIMS) as part of CORDAP’s Scoping Studies (a series of planning sessions and technology roadmap studies to shape our funding priorities). Our aim was to develop a visionary roadmap, offering recommendations on how to prioritise assisted evolution in R&D investment in the future. Assisted evolution is the use of human interventions to speed up the natural evolutionary process. It may allow coral species to adapt faster than they would if left unaided, allowing reefs and corals to keep better pace with the ocean’s environmental changes. The first step in creating this strategy was to pinpoint where we are now in our understanding regarding the potential and impacts of assisted evolution on enhancing coral tolerance to stress conditions like ocean warming. Our experts unanimously agreed that assisted evolution methods cannot be understood and evaluated without a solid foundational understanding of natural adaptation, and identified some knowledge gaps that can be closed with relatively minimal effort and others that will require substantial investment of time and resources. Key Findings: - Standardising methods, experimental designs, species selection guidelines, and terminologies will help to understand natural adaptation and assisted evolution more rapidly. - Long-term funding is critical to facilitate multigenerational studies, which are needed to deliver essential but largely missing information about coral evolution. Building the best pathway for research and investment This roadmap sets out tangible recommendations for future investment and research, to help fill critical knowledge gaps that could assist natural adaptation and evolution of coral reefs in a warming world. Overall, the roadmap recommends investment in a mixed portfolio of R&D, ranging from technologies with lower perceived risks to those with higher percieved risks and longer R&D horizons. This strategy is advised because of the uncertainty around future heating trajectories and thus requirements for enhancement of tolerance. The roadmap outlined four main areas of work that need to be undertaken: 1. Leading global coordination and synthesis. Recommendation: Building global infrastructure to support research would dramatically accelerate the generation of knowledge around the natural and assisted evolution of corals. This could include compiling and committing to a set of standards and methods that will allow more studies to be used in predictive models, as well as establishing a global resource-sharing network and database to facilitate meta-analysis and synthesis. 2. Optimising generation and use of knowledge. Recommendation: Make sure new studies are well designed and timely. Optimize published and future studies by characterizing relationships between heat stress metrics and other facets of coral fitness. Having funding set aside to be able to quickly respond to bleaching events will ensure vital knowledge is captured rather than lost if and when those events occur. 3. Filling critical knowledge gaps in multigenerational coral data in the laboratory and field. Recommendation: Given the slow-growing nature of coral, longer-term funding would allow researchers to gain critical knowledge needed to estimate the multi-generational benefits and risks of implementing assisted evolution methods in the wild. Standardised approaches repeated in different parts of the world would add confidence to generalise those results. 4. Supporting the advance of existing and new technologies. Recommendation: Methods that may yield a larger effect (e.g., gene editing, hybridisation between species, and assisted migration) are also potentially of greater risk and would need considerable R&D. Expanding support for some of the riskier long-term projects currently being overlooked, could potentially offer a greater return on investment, but should be balanced with continued investment in less risky technologies. CORDAP will be using these recommendations to prepare new accelerator program and we believe that they will assist academia in understanding gaps and needs for future research as well as helping to guide funding agencies on where their money will be most effective. The roadmap identifies the funding structures and research priorities that are most likely to yield the knowledge needed to ensure that assisted evolution methods can be implemented effectively. Ultimately, conserving and restoring coral reefs in warming climates will require an inclusive infrastructure involving many partners at a local, national, and international level.

Description: Current research highlights the importance of associated microbes in contributing to the functioning, health, and even adaptation of their animal, plant, and fungal hosts. As such, we are witnessing a shift in research that moves away from focusing on the eukaryotic host sensu stricto to research into the complex conglomerate of the host and its associated microorganisms (i.e., microbial eukaryotes, archaea, bacteria, and viruses), the so-called metaorganism, as the biological entity. While recent research supports and encourages the adoption of such an integrative view, it must be understood that microorganisms are not involved in all host processes and not all associated microorganisms are functionally important. As such, our intention here is to provide a critical review and evaluation of perspectives and limitations relevant to studying organisms in a metaorganism framework and the functional toolbox available to do so. We note that marker gene-guided approaches that primarily characterize microbial diversity are a first step in delineating associated microbes but are not sufficient to establish proof of their functional relevance. More sophisticated tools and experiments are necessary to reveal the specific functions of associated microbes. This can be accomplished through the study of metaorganisms in less complex environments, the targeted manipulation of microbial associates, or work at the mechanistic level with the toolbox available in model systems. We conclude that the metaorganism framework is a powerful new concept to help provide answers to longstanding biological questions such as the evolution and ecology of organismal complexity and the importance of organismal symbioses to ecosystem functioning. The intricacy of the metaorganism requires a holistic framework combining reductionist and integrative approaches to resolve metaorganism identities and to disclose the various roles that microorganisms play in the biology of their hosts.

Description: It is now recognised that the biology of almost any organism cannot be fully understood without recognising the existence and potential functional importance of associated microbes. Arguably, the emergence of this holistic viewpoint may never have occurred without the development of a crucial molecular technique, 16S rDNA amplicon sequencing, which allowed microbial communities to be easily profiled across a broad range of contexts. A diverse array of molecular techniques are now used to profile microbial communities, infer their evolutionary histories, visualise them in host tissues, and measure their molecular activity. In this review, we examine each of these categories of measurement and inference with a focus on the questions they make tractable, and the degree to which their capabilities and limitations shape our view of the holobiont.

Description: Global biodiversity loss and mass extinction of species are two of the most critical environmental issues the world is currently facing, resulting in the disruption of various ecosystems central to environmental functions and human health. Microbiome-targeted interventions, such as probiotics and microbiome transplants, are emerging as potential options to reverse deterioration of biodiversity and increase the resilience of wildlife and ecosystems. However, the implementation of these interventions is urgently needed. We summarize the current concepts, bottlenecks and ethical aspects encompassing the careful and responsible management of ecosystem resources using the microbiome (termed microbiome stewardship) to rehabilitate organisms and ecosystem functions. We propose a real-world application framework to guide environmental and wildlife probiotic applications. This framework details steps that must be taken in the upscaling process while weighing risks against the high toll of inaction. In doing so, we draw parallels with other aspects of contemporary science moving swiftly in the face of urgent global challenges.