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Allemand, D.

Publications and source records attributed to Allemand, D..

9 recordsLinked to original sources

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↗

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↗

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↗

Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals

Stony corals form the foundation of coral reef ecosystems. Their phylogeny is characterized by a deep evolutionary divergence that separates corals into a robust and complex clade dating back to at least 245 mya. However, the genomic consequences and clade-specific evolution remain unexplored. In this study we have produced the genome of a robust coral, Stylophora pistillata, and compared it to the available genome of a complex coral, Acropora digitifera. We conducted a fine-scale gene-based analysis focusing on ortholog groups. Among the core set of conserved proteins, we found an emphasis on processes related to the cnidarian-dinoflagellate symbiosis. Similarly, genes associated with the algal symbiosis were also independently expanded in both species, but both corals diverged on the identity of ortholog groups expanded, and we found uneven expansions in genes associated with innate immunity and stress response. Our analyses demonstrate that coral genomes can be surprisingly disparate. Importantly, if the patterns elucidated here are representative of differences between corals from the robust and complex clade, the ability of a coral to respond to climate change may be dependent on its clade association.

genomics↗

Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral

Over the last century, the anthropogenic production of CO2 has led to warmer (+0.74 {degrees}C) and more acidic (-0.1 pH) oceans1, resulting in increasingly frequent and severe mass bleaching events worldwide that precipitate global coral reef decline2,3. To mitigate this decline, proposals to augment the stress tolerance of corals through genetic and non-genetic means have been gaining traction4. Work on model systems has shown that environmentally induced alterations in DNA methylation can lead to phenotypic acclimatization5,6. While DNA methylation has been observed in corals7-10, its potential role in phenotypic plasticity has not yet been described. Here, we show that, similar to findings in mice11, DNA methylation significantly reduces spurious transcription in the Red Sea coral Stylophora pistillata, suggesting the evolutionary conservation of this essential mechanism in corals. Furthermore, we find that DNA methylation also reduces transcriptional noise by fine-tuning the expression of highly expressed genes. Analysis of DNA methylation patterns of corals subjected to long-term pH stress showed widespread changes in pathways regulating cell cycle and body size. Correspondingly, we found significant increases in cell and polyp sizes that resulted in more porous skeletons, supporting the maintenance of linear extension rates under conditions of reduced calcification. These findings suggest an epigenetic component in phenotypic acclimatization, providing corals with an additional mechanism to cope with climate change.

ecology↗