The algal endosymbiont
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Durusdinium trenchii enhances the resilience of coral reefs under thermal stress.D. trenchii can live freely or in endosymbiosis, and the analysis of genetic markers suggests that this species has undergone whole-genome duplication (WGD). However, the evolutionary mechanisms that underpin the thermotolerance of this species are largely unknown. Here, we present genome assemblies for twoD. trenchii isolates, confirm WGD in these taxa, and examine how selection has shaped the duplicated genome regions using gene expression data. We assess how the free-living versus endosymbiotic lifestyles have contributed to the retention and divergence of duplicated genes, and how these processes have enhanced the thermotolerance ofD. trenchii . Our combined results suggest that lifestyle is the driver of post-WGD evolution inD. trenchii , with the free-living phase being the most important, followed by endosymbiosis. Adaptations to both lifestyles likely enabledD. trenchii to provide enhanced thermal stress protection to the host coral.Free, publicly-accessible full text available July 19, 2025 -
Abstract Dinoflagellates in the family Symbiodiniaceae are taxonomically diverse, predominantly symbiotic lineages that are well-known for their association with corals. The ancestor of these taxa is believed to have been free-living. The establishment of symbiosis (i.e. symbiogenesis) is hypothesized to have occurred multiple times during Symbiodiniaceae evolution, but its impact on genome evolution of these taxa is largely unknown. Among Symbiodiniaceae, the genus Effrenium is a free-living lineage that is phylogenetically positioned between two robustly supported groups of genera within which symbiotic taxa have emerged. The apparent lack of symbiogenesis in Effrenium suggests that the ancestral features of Symbiodiniaceae may have been retained in this lineage. Here, we present de novo assembled genomes (1.2–1.9 Gbp in size) and transcriptome data from three isolates of Effrenium voratum and conduct a comparative analysis that includes 16 Symbiodiniaceae taxa and the other dinoflagellates. Surprisingly, we find that genome reduction, which is often associated with a symbiotic lifestyle, predates the origin of Symbiodiniaceae. The free-living lifestyle distinguishes Effrenium from symbiotic Symbiodiniaceae vis-à-vis their longer introns, more-extensive mRNA editing, fewer (~30%) lineage-specific gene sets, and lower (~10%) level of pseudogenization. These results demonstrate how genome reduction and the adaptation to distinct lifestyles intersect to drive diversification and genome evolution of Symbiodiniaceae.
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Dinoflagellates in the order Suessiales include the family Symbiodiniaceae, which have essential roles as photosymbionts in corals, and their cold-adapted sister group,
Polarella glacialis . These diverse taxa exhibit extensive genomic divergence, although their genomes are relatively small (haploid size < 3 Gbp) when compared with most other free-living dinoflagellates. Different strains of Symbiodiniaceae form symbiosis with distinct hosts and exhibit different regimes of gene expression, but intraspecific whole-genome divergence is poorly understood. Focusing on three Symbiodiniaceae species (the free-livingEffrenium voratum and the symbioticSymbiodinium microadriaticum andDurusdinium trenchii ) and the free-living outgroupP. glacialis , for which whole-genome data from multiple isolates are available, we assessed intraspecific genomic divergence with respect to sequence and structure. Our analysis, based on alignment and alignment-free methods, revealed a greater extent of intraspecific sequence divergence in Symbiodiniaceae than inP. glacialis . Our results underscore the role of gene duplication in generating functional innovation, with a greater prevalence of tandemly duplicated single-exon genes observed in the genomes of free-living species than in symbionts. These results demonstrate the remarkable intraspecific genomic divergence in dinoflagellates under the constraint of reduced genome sizes, shaped by genetic duplications and symbiogenesis events during the diversification of Symbiodiniaceae. -
Dinoflagellates of the family Symbiodiniaceae are crucial photosymbionts in corals and other marine organisms. Of these, Cladocopium goreaui is one of the most dominant symbiont species in the Indo-Pacific. Here, we present an improved genome assembly of C. goreaui combining new long-read sequence data with previously generated short-read data. Incorporating new full-length transcripts to guide gene prediction, the C. goreaui genome (1.2 Gb) exhibits a high extent of completeness (82.4% based on BUSCO protein recovery) and better resolution of repetitive sequence regions; 45,322 gene models were predicted, and 327 putative, topologically associated domains of the chromosomes were identified. Comparison with other Symbiodiniaceae genomes revealed a prevalence of repeats and duplicated genes in C. goreaui, and lineage-specific genes indicating functional innovation. Incorporating 2,841,408 protein sequences from 96 taxonomically diverse eukaryotes and representative prokaryotes in a phylogenomic approach, we assessed the evolutionary history of C. goreaui genes. Of the 5246 phylogenetic trees inferred from homologous protein sets containing two or more phyla, 35–36% have putatively originated via horizontal gene transfer (HGT), predominantly (19–23%) via an ancestral Archaeplastida lineage implicated in the endosymbiotic origin of plastids: 10–11% are of green algal origin, including genes encoding photosynthetic functions. Our results demonstrate the utility of long-read sequence data in resolving structural features of a dinoflagellate genome, and highlight how genetic transfer has shaped genome evolution of a facultative symbiont, and more broadly of dinoflagellates.more » « less
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Dinoflagellates of the family Symbiodiniaceae are predominantly essential symbionts of corals and other marine organisms. Recent research reveals extensive genome sequence divergence among Symbiodiniaceae taxa and high phylogenetic diversity hidden behind subtly different cell morphologies. Using an alignment-free phylogenetic approach based on sub-sequences of fixed length k (i.e. k -mers), we assessed the phylogenetic signal among whole-genome sequences from 16 Symbiodiniaceae taxa (including the genera of Symbiodinium , Breviolum , Cladocopium , Durusdinium and Fugacium ) and two strains of Polarella glacialis as outgroup. Based on phylogenetic trees inferred from k -mers in distinct genomic regions (i.e. repeat-masked genome sequences, protein-coding sequences, introns and repeats) and in protein sequences, the phylogenetic signal associated with protein-coding DNA and the encoded amino acids is largely consistent with the Symbiodiniaceae phylogeny based on established markers, such as large subunit rRNA. The other genome sequences (introns and repeats) exhibit distinct phylogenetic signals, supporting the expected differential evolutionary pressure acting on these regions. Our analysis of conserved core k -mers revealed the prevalence of conserved k -mers (>95% core 23-mers among all 18 genomes) in annotated repeats and non-genic regions of the genomes. We observed 180 distinct repeat types that are significantly enriched in genomes of the symbiotic versus free-living Symbiodinium taxa, suggesting an enhanced activity of transposable elements linked to the symbiotic lifestyle. We provide evidence that representation of alignment-free phylogenies as dynamic networks enhances the ability to generate new hypotheses about genome evolution in Symbiodiniaceae. These results demonstrate the potential of alignment-free phylogenetic methods as a scalable approach for inferring comprehensive, unbiased whole-genome phylogenies of dinoflagellates and more broadly of microbial eukaryotes.more » « less
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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.more » « less