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Background: Cladocopium infistulum (Symbiodiniaceae) is a dinoflagellate specialized to live in symbiosis with western Pacific giant clams (Tridacnidae). Unlike coral-associated symbionts, which reside within the host cells, C. infistulum inhabits the extracellular spaces of the clam's digestive diverticula. It is phylogenetically basal to a large species complex of stress-tolerant Cladocopium, many of which are associated with important reef-building corals in the genus Porites. This close phylogenetic relationship may explain why C. infistulum exhibits high thermotolerance relative to other tridacnid symbionts. Moreover, past analyses of microsatellite loci indicated that Cladocopium underwent whole-genome duplication prior to the adaptive radiations that led to its present diversity., Results: A draft genome assembly of C. infistulum was produced using long- and short-read sequences to explore the genomic basis for adaptations underlying thermotolerance and extracellular symbiosis among dinoflagellates and to look for evidence of genome duplication. Comparison to three other Cladocopium genomes revealed no obvious over-representation of gene groups or families whose functions would be important for maintaining C. infistulum's unique physiological and ecological properties. Preliminary analyses support the existence of partial or whole-genome duplication among Cladocopium, but additional high-quality genomes are required to substantiate these findings., Conclusion: Although this investigation of Cladocopium infistulum revealed no patterns diagnostic of heat tolerance or extracellular symbiosis in terms of overrepresentation of gene functions or genes under selection, it provided a valuable genomic resource for comparative analyses. It also indicates that ecological divergence among Cladocopium species, and potentially among other dinoflagellates, is partially governed by mechanisms other than gene content. Thus, additional high-quality, multiomic data are needed to explore the molecular basis of key phenotypes among symbiotic microalgae., (© 2024. The Author(s).)

The holobiont concept (i.e., multiple living beings in close symbiosis with one another and functioning as a unit) is revolutionizing our understanding of biology, especially in marine systems. The earliest marine holobiont was likely a syntrophic partnership of at least two prokaryotic members. Since then, symbiosis has enabled marine organisms to conquer all ocean habitats through the formation of holobionts with a wide spectrum of complexities. However, most scientific inquiries have focused on isolated organisms and their adaptations to specific environments. In this review, we attempt to illustrate why a holobiont perspective-specifically, the study of how numerous organisms form a discrete ecological unit through symbiosis-will be a more impactful strategy to advance our understanding of the ecology and evolution of marine life. We argue that this approach is instrumental in addressing the threats to marine biodiversity posed by the current global environmental crisis.

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians ( e.g ., corals, octocorals, sea anemones, jellyfish), other marine invertebrates ( e.g. , sponges, molluscs, flatworms), and protists ( e.g ., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships., Competing Interests: Anastazia T. Banaszak and James Davis Reimer are Academic Editors for PeerJ., (© 2023 Davies et al.)

Modern microbial taxonomy generally relies on the use of single marker genes or sets of concatenated genes to generate a framework for the delineation and classification of organisms at different taxonomic levels. However, given that DNA is the 'blueprint of life', and hence the ultimate arbiter of taxonomy, classification systems should attempt to use as much of the blueprint as possible to capture a comprehensive phylogenetic signal. Recent analysis of whole-genome sequences from coral reef symbionts (dinoflagellates of the family Symbiodiniaceae) and other microalgal groups has uncovered extensive divergence not recognised by current algal taxonomic approaches. In the era of 'sequence everything', we argue that whole-genome data are pivotal to guide informed taxonomic inference, particularly for microbial eukaryotes., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

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.

Inferring phylogenetic relationships among hundreds or thousands of microbial genomes is an increasingly common task. The conventional phylogenetic approach adopts multiple sequence alignment to compare gene-by-gene, concatenated multigene or whole-genome sequences, from which a phylogenetic tree would be inferred. These alignments follow the implicit assumption of full-length contiguity among homologous sequences. However, common events in microbial genome evolution (e.g., structural rearrangements and genetic recombination) violate this assumption. Moreover, aligning hundreds or thousands of sequences is computationally intensive and not scalable to the rate at which genome data are generated. Therefore, alignment-free methods present an attractive alternative strategy. Here we describe a scalable alignment-free strategy to infer phylogenetic relationships using complete genome sequences of bacteria and archaea, based on short, subsequences of length k (k-mers). We describe how this strategy can be extended to infer evolutionary relationships beyond a tree-like structure, to better capture both vertical and lateral signals of microbial evolution.

Background: Dinoflagellates are taxonomically diverse and ecologically important phytoplankton that are ubiquitously present in marine and freshwater environments. Mostly photosynthetic, dinoflagellates provide the basis of aquatic primary production; most taxa are free-living, while some can form symbiotic and parasitic associations with other organisms. However, knowledge of the molecular mechanisms that underpin the adaptation of these organisms to diverse ecological niches is limited by the scarce availability of genomic data, partly due to their large genome sizes estimated up to 250 Gbp. Currently available dinoflagellate genome data are restricted to Symbiodiniaceae (particularly symbionts of reef-building corals) and parasitic lineages, from taxa that have smaller genome size ranges, while genomic information from more diverse free-living species is still lacking., Results: Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. We found that about 68% of the genomes are composed of repetitive sequence, with long terminal repeats likely contributing to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp). For each genome, guided using full-length transcriptome data, we predicted > 50,000 high-quality protein-coding genes, of which ~40% are in unidirectional gene clusters and ~25% comprise single exons. Multi-genome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial origin of ice-binding domains in cold-adapted dinoflagellates., Conclusions: Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Because most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light polar environments. These genomes provide a foundational reference for future research on dinoflagellate evolution.

Coral reefs are sustained by symbioses between corals and symbiodiniacean dinoflagellates. These symbioses vary in the extent of their permanence in and specificity to the host. Although dinoflagellates are primarily free-living, Symbiodiniaceae diversified mainly as symbiotic lineages. Their genomes reveal conserved symbiosis-related gene functions and high sequence divergence. However, the evolutionary mechanisms that underpin the transition from the free-living lifestyle to symbiosis remain poorly understood. Here, we discuss the genome evolution of Symbiodiniaceae in diverse ecological niches across the broad spectrum of symbiotic associations, from free-living to putative obligate symbionts. We pose key questions regarding genome evolution vis-à-vis the transition of dinoflagellates from free-living to symbiotic and propose strategies for future research to better understand coral-dinoflagellate and other eukaryote-eukaryote symbioses., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

[This corrects the article DOI: 10.1038/s42003-018-0098-3.].

Symbiosis between dinoflagellates of the genus Symbiodinium and reef-building corals forms the trophic foundation of the world's coral reef ecosystems. Here we present the first draft genome of Symbiodinium goreaui (Clade C, type C1: 1.03 Gbp), one of the most ubiquitous endosymbionts associated with corals, and an improved draft genome of Symbiodinium kawagutii (Clade F, strain CS-156: 1.05 Gbp) to further elucidate genomic signatures of this symbiosis. Comparative analysis of four available Symbiodinium genomes against other dinoflagellate genomes led to the identification of 2460 nuclear gene families (containing 5% of Symbiodinium genes) that show evidence of positive selection, including genes involved in photosynthesis, transmembrane ion transport, synthesis and modification of amino acids and glycoproteins, and stress response. Further, we identify extensive sets of genes for meiosis and response to light stress. These draft genomes provide a foundational resource for advancing our understanding of  Symbiodinium biology and the coral-algal symbiosis., Competing Interests: The authors declare no competing interests.

Symbiodinium is best-known as the photosynthetic symbiont of corals, but some clades are symbiotic in other organisms or include free-living forms. Identifying similarities and differences among these clades can help us understand their relationship with corals, and thereby inform on measures to manage coral reefs in a changing environment. Here, using sequences from 24 publicly available transcriptomes and genomes of Symbiodinium, we assessed 78,389 gene families in Symbiodinium clades and the immediate outgroup Polarella glacialis, and identified putative overrepresented functions in gene families that (1) distinguish Symbiodinium from other members of Order Suessiales, (2) are shared by all of the Symbiodinium clades for which we have data, and (3) based on available information, are specific to each clade. Our findings indicate that transmembrane transport, mechanisms of response to reactive oxygen species, and protection against UV radiation are functions enriched in all Symbiodinium clades but not in P. glacialis. Enrichment of these functions indicates the capability of Symbiodinium to establish and maintain symbiosis, and to respond and adapt to its environment. The observed differences in lineage-specific gene families imply extensive genetic divergence among clades. Our results provide a platform for future investigation of lineage- or clade-specific adaptation of Symbiodinium to their environment.