bioRxiv Science⌕ Search

Biology subjects

Boissin, E.

Publications and source records attributed to Boissin, E..

13 recordsLinked to original sources

Host genetics structure prokaryotic and Symbiodiniaceae assemblages and their co-variation in sympatric fire coral species

Host-symbiont specificity and environmental filtering are important constraints on holobiont structure and resilience. Yet, resolving the extent of these constraints requires moving beyond species-level resolution, as intraspecific host genetic diversity can further modulate symbiotic associations in ways that remain poorly understood. Here, we resolved host genetic identity at the subspecies level to disentangle drivers of symbiotic plasticity in three sympatric fire coral species (Millepora cf. exaesa, M. tenera, and M. cf. platyphylla) across three adjacent but environmentally distinct habitats on Reunion Island (inner and outer reef flats, reef slope,). Symbiont assemblages were primarily structured by host species and genotypes, with a stronger genetic influence on Symbiodiniaceae than on prokaryotic assemblages, while habitat played a significant but secondary role. Symbiodiniaceae communities were dominated by Symbiodinium A16 and A3 radiations, showing marked specificity across species and habitats. All Millepora species consistently associated with the Spirochaetaceae, Kiloniellaceae and Desulfobacteraceae bacterial families across all habitats, suggesting evolutionarily maintained core associations. Both symbiotic compartments shifted across every habitat in host-specific ways, demonstrating microbiome plasticity to local environmental conditions. Integration of symbiont sequence data (ITS2 and 16S) further revealed genotype-specific co-variation patterns, with some genotypes maintaining stable and co-varying symbionts across clones, while others exhibited greater plasticity. Together, our results indicate that fire coral holobionts acquire symbionts from locally available pools based primarily on their specific genetic compatibility. This study sheds light on how fine-scale host identity and environment jointly shape unique host-symbiont associations contributing to the ecological success of these sympatric coral species.

ecology↗

Diversity, host-specificity, and environmental drivers of the coral reef eukaryome

Coral reefs are among the most diverse ecosystems on Earth, yet the diversity and structure of their associated microeukaryotic communities remain poorly resolved. We characterized reef-associated eukaryomes across 113 reefs spanning the Pacific Ocean using more than 6,300 samples from corals, seawater, and sediments during the Tara Pacific expedition. We identified [~]121,000 eukaryotic ASVs, revealing one of Earths largest undocumented reservoirs of eukaryotic diversity; over 80% of the recovered diversity was previously undetected in global ocean surveys and fewer than 2% of sequences matched reference databases. Reef habitats supported highly distinct communities, with sediments and seawater harboring 20-40-fold higher richness than corals. Unexpectedly, coral-associated communities across 29 host lineages were consistently dominated by small metazoans, particularly demosponges and maxillopods, identifying these taxa as pervasive and previously unrecognized components of coral eukaryomes alongside Apicomplexa. Across the Pacific, eukaryome composition was strongly structured by environmental gradients, with thermal stress emerging as the primary driver of community turnover. Together, these results identify coral reefs as a globally important reservoir of hidden eukaryotic diversity and reveal the reef eukaryome as a sensitive indicator of ecosystem reorganization under climate change.

systems biology↗

HIDDEN APICOMPLEXAN PARASITE DIVERSITY LINKS CORAL AND PLANKTON MICROBIOMES ACROSS REEF SEASCAPES

Parasitism is one of the most widespread trophic strategies in nature, though its diversity and ecological distribution in marine ecosystems remain poorly characterized. Apicomplexa are a major clade of obligate parasites best known for medically important taxa, yet their diversity and distribution in the ocean is still largely unresolved. Here, we used metabarcoding data from the Tara expeditions to investigate the diversity, distribution, and environmental drivers of Apicomplexa across coral reef ecosystems and adjacent oceanic habitats. By integrating samples spanning planktonic communities, coral tissues, and marine sediments across multiple oceanic regions, we substantially expand the known phylogenetic breadth of marine apicomplexans. Although apicomplexans were generally low in relative abundance, they were widely distributed across marine environments. Community composition differed markedly among habitats. Corallicolid lineages were consistently associated with coral hosts, whereas planktonic samples harbored a greater diversity of apicomplexans, dominated by crustacean-associated gregarines. Sediments contained particularly high apicomplexan richness, including several poorly characterized groups. Capitalizing on the pan-Pacific transect of the expedition, we resolved biogeographic patterns in apicomplexan diversity across ocean basins: tropical regions showed the highest overall diversity, while polar environments contained distinct apicomplexan assemblages not detected in other ocean biomes. Together, these results highlight the extensive and previously underappreciated diversity of marine Apicomplexa and demonstrate that integrating multiple marine biomes is essential for resolving the phylogenetic and ecological breadth of parasitism in the ocean.

genomics↗

Ocean-scale transcriptomic analysis of corallicolids (Apicomplexa) reveals their ubiquity and molecular interactions with Pocillopora corals.

Corals are complex holobionts, encompassing numerous prokaryotes, viruses, and protists. This associated microbial community strongly influences coral health and its resilience to global ocean warming. Corallicolid apicomplexans are widespread coral-infecting parasites, yet their impact on the coral host remains poorly understood. This knowledge gap largely stems from the low abundance of these parasites in coral tissues, which makes them difficult to isolate and access to their genetic material. Here we analyzed nearly 1,000 Pocillopora coral colonies collected from 32 islands during the Tara Pacific expedition to identify the drivers of corallicolid prevalence and abundance. Corallicolids were detected in almost all Pocillopora colonies with variable relative abundances between islands. The high abundance of specific corallicolid populations correlates with seawater temperature and levels of host protein carbonylation. We used a large collection of 297 metatranscriptomes to assemble a corallicolid transcriptome and we identified apicomplexan parasite signature genes, including the GRA9 and PV2 confirming the close phylogenetic relationship with the family of Eimeriidae. Gene expression patterns indicate that the high abundance of corallicolids correlates with a high transcription of genes encoding apical complex proteins and genes involved in the control of host immune defenses. Overall, this study provides new insights into corallicolid biology and its interaction with the coral host by combining a newly generated transcriptome with a large-scale sampling of Pocillopora corals across the Pacific Ocean.

genomics↗

Genome-resolved diversity and biosynthetic potential of the coral reef microbiome

Coral reefs are marine biodiversity hotspots that provide a wide range of ecosystem services. They are also reservoirs of bioactive compounds, many of which are produced by microbial symbionts associated with reef invertebrate hosts. However, for the keystone species of coral reefs--the reef-building corals themselves--we still lack a systematic assessment of their microbially encoded biosynthetic potential, and thus the molecular resources that may be at stake due to the alarming decline in reef biodiversity and cover. Here, we analysed microbial genomes reconstructed from 820 reef-building coral samples of three representative coral genera collected at 99 reefs across 32 islands during a two-year expedition throughout the Pacific Ocean (Tara Pacific). By contextualising our analyses with the microbiomes of other reef species, we found that genomic information was previously available for only 10% of the 4,224 microbial species overall and for less than 1% of the 645 species exclusively identified in Tara Pacific samples. We found reef-building coral microbiomes to be host-specific and their biosynthetic potential to rival or even surpass that found in traditional targets for natural product discovery, such as sponges and soft corals. Fire corals were not only particularly diverse in microbially encoded biosynthetic gene clusters (BGCs), but also in BGC-rich bacteria, including Acidobacteriota spp., which have been recently highlighted for their promising natural product repertoire. Together, this study unveils new candidate sources for bioactive compound discovery, prioritises targets for microbial isolation, and underscores the importance of conservation efforts by linking macro-organismal biodiversity loss to host-specific microbiomes and their biotechnological potential.

microbiology↗

Algal symbioses with fire corals demonstrate host genotype specificity and niche adaptation at subspecies resolution

Corals share an intimate relationship with photosynthetic dinoflagellates that contribute to the biology of the emerging metaorganism. While many coral-algal associations exhibit high host fidelity, the extent of this specificity under environmental change remains to be fully understood and is a prerequisite to forecasting the adaptive potential of this obligate symbiosis. Here, we disentangled the contribution of host genotype and environment on governing coral-algae associations by working at subspecies resolution. We used fine-scale genotyping of algal symbionts from 198 fire coral colonies (Millepora cf. platyphylla) that map to ten distinct sexually produced clonal host genotypes across three environmentally distinct reef habitats. Based on microalgal ITS2 genotyping, we show that algal-host specificity extends down to the Symbiodiniaceae subspecies level in a natural reef environment. Closely related Symbiodinium (A7)-dominated algal assemblages almost perfectly mapped to fire coral host genotype. Furthermore, identification of host genotype- and habitat-specific Symbiodinium alga suggest the presence of algal phenotypic diversity even at this taxonomic resolution (i.e., within Symbiodinium A7), which may aid environmental niche adaptation of the metaorganism. Our results suggest that the here-identified Millepora-Symbiodinium associations are co-evolved to match their prevailing environment. Thus, despite the presence of rarer host generalist Cladocopium algae, scope for environmentally induced modification of the cnidarian-algal association is likely constrained by host genotype.

evolutionary biology↗

Graphicacy across age, education, and culture: a new tool to assess intuitive graphics skills

Data plots are widely used in science, journalism and politics, since they efficiently allow to depict a large amount of information. Graphicacy, the ability to understand graphs, thus became a fundamental cultural skill. Here, we introduce a new measure of graphicacy that assesses the ability to detect a trend in noisy scatterplots ("does this graph go up or down?"). In 3943 educated participants, responses vary as a sigmoid function of the t-value that a statistician would compute to detect a significant trend. We find a minimum level of core graphicacy even in unschooled participants living in remote Namibian villages (N=87) and 6-year-old 1st-graders who never read a graph (N=27). However, the sigmoid slope (the "graphicacy index") varies across participants, increases with education, and tightly correlates with statistical knowledge, showing that experience contributes to refining graphical intuitions. Our tool is publicly available online and allows to quickly evaluate intuitive graphics skills. STATEMENT OF RELEVANCEThe rising cost of gas, the number of Covid deaths, the evolution of temperatures during the summer months: we often face graphs depicting these phenomena. The scientific literature has shown that human adults can intuit, within milliseconds, the statistical trend of these graphs. However, we do not know if these intuitions generalized to unschooled people and, most importantly, how to measure their variations in the population. In this study we show that intuitive graphics skills are present even in 6-year-old children who never saw a graph and in the Himba of Namibia, an indigenous people with no access to formal schooling. Furthermore, we developed a quantitative assessment of such intuitive graphics skills (which we called the "graphicacy index"), that everyone can easily obtain for free, through a short (10 minutes) online test: https://neurospin-data.cea.fr/exp/lorenzo-ciccione/graphicacy-index/. In summary, our study provides the first attempt to formally quantify human intuitions of statistical graphs.

scientific communication and education↗

From genome wide SNPs to genomic islands of differentiation: the quest for species diagnostic markers in two scleractinian corals, Pocillopora and Porites

Coral reefs are of paramount importance in marine ecosystems, where they provide support for a large part of the biodiversity. Being quite sensitive to global changes, they are therefore the prime targets for biodiversity conservation policies. However, such conservation goals require accurate species identification, which are notoriously difficult to get in these highly morphologically variable organisms, rich in cryptic species. There is an acute need for easy-to-use and resolutive species diagnostic molecular markers. The present study builds on the huge sequencing effort developed during the TARA Pacific expedition to develop a genotyping strategy to assign coral samples to the correct species within two coral genera (Porites and Pocillopora). For this purpose, we developed a technique that we called "Divergent Fragment" based on the sequencing of a less than 2kb long diagnostic genomic fragment determined from the metagenomic data of a subset of the corals collected. This method has proven to be rapid, resolvable and cost-effective. Sequencing of PCR fragments nested along the species diagnostic fragment allowed us to assign 232 individuals of the genus Pocillopora and 247 individuals of the genus Porites to previously identified independent genetic lineages (i.e. species). This genotyping method will allow to fully analyze the coral samples collected across the Pacific during the Tara Pacific expedition and opens technological perspectives in the field of population genomics-guided conservation.

evolutionary biology↗

Disparate patterns of genetic divergence in three widespread corals across a pan-Pacific environmental gradient highlights species-specific adaptation trajectories.

Tropical coral reefs are among the worst affected ecosystems by climate change with predictions ranging between a 70-90% loss of reefs in the coming decades. Effective conservation strategies that maximize ecosystem resilience, and potential for recovery, must be informed by the accurate characterization of extant genetic diversity and population structure together with an understanding of the adaptive potential of keystone species. Here, we analyzed samples from the Tara Pacific Expedition (2016 to 2018) that completed an 18,000 km longitudinal transect of the Pacific Ocean sampling three widespread corals - Pocillopora meandrina, Porites lobata, and Millepora cf. platyphylla - across 33 sites from 11 islands. Using deep metagenomic sequencing of 269 colonies in conjunction with morphological analyses and climate variability data we can show that the sampled transect encompasses multiple morphologically cryptic species that exhibit disparate biogeographic patterns, and most importantly, distinct evolutionary patterns, despite exposure to identical environmental regimes. Our findings demonstrate on a basin-scale that evolutionary trajectories are species-specific and complex, and can only in part be predicted from the environment. This highlights that conservation strategies must integrate multi-species investigations to consider the distinct genomic footprints shaped by selection as well as the genetic potential for adaptive change.

genetics↗

Open science resources from the Tara Pacific expedition across coral reef and surface ocean ecosystems

AbstractThe Tara Pacific expedition (2016-2018) sampled coral ecosystems around 32 islands in the Pacific Ocean and the ocean surface waters at 249 locations, resulting in the collection of nearly 58,000 samples. The expedition was designed to systematically study warm coral reefs and included the collection of corals, fish, plankton, and seawater samples for advanced biogeochemical, molecular, and imaging analysis. Here we provide a complete description of the sampling methodology, and we explain how to explore and access the different datasets generated by the expedition. Environmental context data were obtained from taxonomic registries, gazetteers, almanacs, climatologies, operational biogeochemical models, and satellite observations. The quality of the different environmental measures has been validated not only by various quality control steps but also through a global analysis allowing the comparison with known environmental large-scale structures. Such a wide released datasets opens the perspective to address a wide range of scientific questions.

ecology↗

Pervasive gene duplications as a major evolutionary driver of coral biology

Over the last decade, several coral genomes have been sequenced allowing a better understanding of these symbiotic organisms threatened by climate change. Scleractinian corals are reef builders and are central to these ecosystems, providing habitat and food to a great diversity of species. In the frame of the Tara Pacific expedition, we generated two coral genomes, Porites lobata and Pocillopora meandrina with vastly improved contiguity that allowed us to study the functional organisation of these genomes. We annotated their gene catalog and report a relatively higher gene number (43,000 and 32,000 genes respectively) than that found in other public coral genome sequences. This finding is explained by a high number of tandemly duplicated genes (almost a third of the predicted genes). We show that these duplicated genes originate from multiple and distinct duplication events throughout the coral lineage. They contribute to the amplification of gene families, mostly related to immune system and disease-resistance, which we suggest to be functionally linked to coral host resilience. At large, we show the importance of duplicated genes to inform the biology of reef-building corals and provide novel avenues to understand and screen for differences in stress resilience.

genomics↗

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 hours. 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.

genomics↗

Dispersal limitations of early life stages and sibling aggregations in a broadcasting Millepora hydrocoral, as revealed by parentage analysis

Dispersal is a critical process for the persistence and productivity of marine populations. For many reef species, there is increasing evidence that local demography and self-recruitment have major consequences on their genetic diversity and adaptation to environmental change. Yet empirical data of dispersal patterns in reef-building species remain scarce. Here, we document the first genetic estimates of local dispersal and self-recruitment in a broadcasting reef-builder, the hydrocoral Millepora platyphylla. Using microsatellite markers, we gathered genotypic information from 3160 georeferenced colonies collected over 9000 m2 of reef in three adjacent habitats in Moorea, French Polynesia; the mid slope, upper slope and back reef. Our parentage analysis revealed a predominance of self-recruitment with 58% of sexual propagules produced locally. Sexual propagules often settled at less than 10 meters from their parents and dispersal events decrease with increasing geographic distance. Limited dispersal among adjacent habitats via cross-reef transport was also detected. Sibship analysis showed that both full and half siblings recruit together on the reef, resulting in sibling aggregations. The identification of local families revealed discrepancies between dispersal patterns of sexual and asexual propagules. Self-recruits are dispersed with along-reef currents and settled in alignment with the location of their parents, while the dispersal of asexual fragments is heavily influenced by wave-driven cross-reef currents. Our findings highlight the importance of self-recruitment together with clonality in stabilising population dynamics, as it can enhance local sustainability and resilience to disturbance, but also raise uncertainties on the widely accepted high dispersal ability of broadcasting reef species.

ecology↗