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The photosynthetic symbionts of corals sustain biodiverse reefs in nutrient-poor, tropical waters. Recent genomic data illuminate the evolution of coral symbionts under genome size constraints and suggest that retention of the facultative lifestyle, widespread among these algae, confers a selective advantage when compared with a strict symbiotic existence. We posit that the coral symbiosis is analogous to a 'bioreactor' that selects winner genotypes and allows them to rise to high numbers in a sheltered habitat prior to release by the coral host. Our observations lead to a novel hypothesis, the 'stepping-stone model', which predicts that local adaptation under both the symbiotic and free-living stages, in a stepwise fashion, accelerates coral alga diversity and the origin of endemic strains and species. 

The integration of multiple ‘omics’ datasets is a promising avenue for answering many important and challenging questions in biology, particularly those relating to complex ecological systems. Whereas, multi-omics was developed using data from model organisms with significant prior knowledge and resources, its application to non-model organisms, such as coral holobionts, is less clear-cut. We explore, in the emerging rice coral model Montipora capitata, the intersection of holobiont transcriptomic, proteomic, metabolomic, and microbiome amplicon data and investigate how well they correlate under high temperature treatment. Using a typical thermal stress regime, we show that transcriptomic and proteomic data broadly capture the stress response of the coral, whereas the metabolome and microbiome datasets show patterns that likely reflect stochastic and homeostatic processes associated with each sample. These results provide a framework for interpreting multi-omics data generated from non-model systems, particularly those with complex biotic interactions among microbial partners. 

Abstract Standing genetic variation is a major driver of fitness and resilience and therefore of fundamental importance for threatened species such as stony corals. We analyzed RNA-seq data generated from 132 Montipora capitata and 119 Pocillopora acuta coral colonies collected from Kāneʻohe Bay, Oʻahu, Hawaiʻi. Our goals were to determine the extent of colony genetic variation and to study reproductive strategies in these two sympatric species. Surprisingly, we found that 63% of the P. acuta colonies were triploid, with putative independent origins of the different triploid clades. These corals have spread primarily via asexual reproduction and are descended from a small number of genotypes, whose diploid ancestor invaded the bay. In contrast, all M. capitata colonies are diploid and outbreeding, with almost all colonies genetically distinct. Only two cases of asexual reproduction, likely via fragmentation, were identified in this species. We report two distinct strategies in sympatric coral species that inhabit the largest sheltered body of water in the main Hawaiian Islands. These data highlight divergence in reproductive behavior and genome biology, both of which contribute to coral resilience and persistence. 

Abstract Dinoflagellates from the family Symbiodiniaceae are phototrophic marine protists that engage in symbiosis with diverse hosts. Their large and distinct genomes are characterized by pervasive gene duplication and large-scale retroposition events. However, little is known about the role and scale of horizontal gene transfer (HGT) in the evolution of this algal family. In other dinoflagellates, high levels of HGTs have been observed, linked to major genomic transitions, such as the appearance of a viral-acquired nucleoprotein that originated via HGT from a large DNA algal virus. Previous work showed that Symbiodiniaceae from different hosts are actively infected by viral groups, such as giant DNA viruses and ssRNA viruses, that may play an important role in coral health. Latent viral infections may also occur, whereby viruses could persist in the cytoplasm or integrate into the host genome as a provirus. This hypothesis received experimental support; however, the cellular localization of putative latent viruses and their taxonomic affiliation are still unknown. In addition, despite the finding of viral sequences in some genomes of Symbiodiniaceae, viral origin, taxonomic breadth, and metabolic potential have not been explored. To address these questions, we searched for putative viral-derived proteins in thirteen Symbiodiniaceae genomes. We found fifty-nine candidate viral-derived HGTs that gave rise to twelve phylogenies across ten genomes. We also describe the taxonomic affiliation of these virus-related sequences, their structure, and their genomic context. These results lead us to propose a model to explain the origin and fate of Symbiodiniaceae viral acquisitions. 

Primary endosymbiosis allowed the evolution of complex life on Earth. In this process, a prokaryote was engulfed and retained in the cytoplasm of another microbe, where it developed into a new organelle (mitochondria and plastids). During organelle evolution, genes from the endosymbiont are transferred to the host nuclear genome, where they must become active despite differences in the genetic nature of the “partner” organisms. Here, we show that in the amoebaPaulinella micropora, which harbors a nascent photosynthetic organelle, the “copy-paste” mechanism of retrotransposition allowed domestication of endosymbiont-derived genes in the host nuclear genome. This duplication mechanism is widespread in eukaryotes and may be a major facilitator for host–endosymbiont integration and the evolution of organelles. 

Abstract Coral bleaching, precipitated by the expulsion of the algal symbionts that provide colonies with fixed carbon is a global threat to reef survival. To protect corals from anthropogenic stress, portable tools are needed to detect and diagnose stress syndromes and assess population health prior to extensive bleaching. Here, medical grade Urinalysis strips, used to detect an array of disease markers in humans, were tested on the lab stressed Hawaiian coral species,Montipora capitata(stress resistant) andPocillopora acuta(stress sensitive), as well as samples from nature that also includedPorites compressa. Of the 10 diagnostic reagent tests on these strips, two appear most applicable to corals: ketone and leukocytes. The test strip results fromM. capitatawere explored using existing transcriptomic data from the same samples and provided evidence of the stress syndromes detected by the strips. We designed a 3D printed smartphone holder and image processing software for field analysis of test strips (TestStripDX) and devised a simple strategy to generate color scores for corals (reflecting extent of bleaching) using a smartphone camera (CoralDX). Our approaches provide field deployable methods, that can be improved in the future (e.g., coral-specific stress test strips) to assess reef health using inexpensive tools and freely available software. 

Abstract Background Dinoflagellates in the family Symbiodiniaceae are important photosynthetic symbionts in cnidarians (such as corals) and other coral reef organisms. Breakdown of the coral-dinoflagellate symbiosis due to environmental stress (i.e. coral bleaching) can lead to coral death and the potential collapse of reef ecosystems. However, evolution of Symbiodiniaceae genomes, and its implications for the coral, is little understood. Genome sequences of Symbiodiniaceae remain scarce due in part to their large genome sizes (1–5 Gbp) and idiosyncratic genome features. Results Here, we present de novo genome assemblies of seven members of the genus Symbiodinium , of which two are free-living, one is an opportunistic symbiont, and the remainder are mutualistic symbionts. Integrating other available data, we compare 15 dinoflagellate genomes revealing high sequence and structural divergence. Divergence among some Symbiodinium isolates is comparable to that among distinct genera of Symbiodiniaceae. We also recovered hundreds of gene families specific to each lineage, many of which encode unknown functions. An in-depth comparison between the genomes of the symbiotic Symbiodinium tridacnidorum (isolated from a coral) and the free-living Symbiodinium natans reveals a greater prevalence of transposable elements, genetic duplication, structural rearrangements, and pseudogenisation in the symbiotic species. Conclusions Our results underscore the potential impact of lifestyle on lineage-specific gene-function innovation, genome divergence, and the diversification of Symbiodinium and Symbiodiniaceae. The divergent features we report, and their putative causes, may also apply to other microbial eukaryotes that have undergone symbiotic phases in their evolutionary history. 

Background Corals, which form the foundation of biodiverse reef ecosystems, are under threat from warming oceans. Reefs provide essential ecological services, including food, income from tourism, nutrient cycling, waste removal, and the absorption of wave energy to mitigate erosion. Here, we studied the coral thermal stress response using network methods to analyze transcriptomic and polar metabolomic data generated from the Hawaiian rice coral Montipora capitata . Coral nubbins were exposed to ambient or thermal stress conditions over a 5-week period, coinciding with a mass spawning event of this species. The major goal of our study was to expand the inventory of thermal stress-related genes and metabolites present in M. capitata and to study gene-metabolite interactions. These interactions provide the foundation for functional or genetic analysis of key coral genes as well as provide potentially diagnostic markers of pre-bleaching stress. A secondary goal of our study was to analyze the accumulation of sex hormones prior to and during mass spawning to understand how thermal stress may impact reproductive success in M. capitata . Methods M. capitata was exposed to thermal stress during its spawning cycle over the course of 5 weeks, during which time transcriptomic and polar metabolomic data were collected. We analyzed these data streams individually, and then integrated both data sets using MAGI (Metabolite Annotation and Gene Integration) to investigate molecular transitions and biochemical reactions. Results Our results reveal the complexity of the thermal stress phenome in M. capitata , which includes many genes involved in redox regulation, biomineralization, and reproduction. The size and number of modules in the gene co-expression networks expanded from the initial stress response to the onset of bleaching. The later stages involved the suppression of metabolite transport by the coral host, including a variety of sodium-coupled transporters and a putative ammonium transporter, possibly as a response to reduction in algal productivity. The gene-metabolite integration data suggest that thermal treatment results in the activation of animal redox stress pathways involved in quenching molecular oxygen to prevent an overabundance of reactive oxygen species. Lastly, evidence that thermal stress affects reproductive activity was provided by the downregulation of CYP-like genes and the irregular production of sex hormones during the mass spawning cycle. Overall, redox regulation and metabolite transport are key components of the coral animal thermal stress phenome. Mass spawning was highly attenuated under thermal stress, suggesting that global climate change may negatively impact reproductive behavior in this species. 

Abstract Degradation and loss of coral reefs due to climate change and other anthropogenic stressors has fueled genomics, proteomics, and genetics research to investigate coral stress response pathways and to identify resilient species, genotypes, and populations to restore these biodiverse ecosystems. Much of the research and conservation effort has understandably focused on the most taxonomically rich regions, such as the Great Barrier Reef in Australia and the Coral Triangle in the western Pacific. These ecosystems are analogous to tropical rainforests that also house enormous biodiversity and complex biotic interactions among different trophic levels. An alternative model ecosystem for studying coral reef biology is the relatively species poor but abundant coral reefs in the Hawaiian Archipelago that exist at the northern edge of the Indo‐Pacific coral distribution. The Hawaiian Islands are the world's most isolated archipelago, geographically isolated from other Pacific reef systems. This region houses about 80 species of scleractinian corals in three dominant genera (Porites,Montipora, andPocillopora). Here we briefly review knowledge about the Hawaiian coral fauna with a focus on our model species, the rice coralMontipora capitata. We suggest that this simpler, relatively isolated reef system provides an ideal platform for advancing coral biology and conservation using multi‐omics and genetic tools.