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.
Genome Evolution of Coral Reef Symbionts as Intracellular Residents
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.
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- Award ID(s):
- 1756616
- PAR ID:
- 10166053
- Date Published:
- Journal Name:
- Trends in ecology evolution
- Volume:
- 34
- Issue:
- 9
- ISSN:
- 0169-5347
- Page Range / eLocation ID:
- 799-805
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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
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null (Ed.)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
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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. -
null (Ed.)Symbiotic relationships enable partners to thrive and survive in habitats where they would either not be as successful, or potentially not exist, without the symbiosis. The coral reef ecosystem, and its immense biodiversity, relies on the symbioses between cnidarians (e.g., scleractinian corals, octocorals, sea anemones, jellyfish) and multiple organisms including dinoflagellate algae (family Symbiodiniaceae), bivalves, crabs, shrimps, and fishes. In this review, we discuss the ramifications of whether coral reef cnidarian symbioses are obligatory, whereby at least one of the partners must be in the symbiosis in order to survive or are facultative. Furthermore, we cover the consequences of cnidarian symbioses exhibiting partner flexibility or fidelity. Fidelity, where a symbiotic partner can only engage in symbiosis with a subset of partners, may be absolute or context dependent. Current literature demonstrates that many cnidarian symbioses are highly obligative and appear to exhibit absolute fidelity. Consequently, for many coral reef cnidarian symbioses, surviving changing environmental conditions will depend on the robustness and potential plasticity of the existing host-symbiont(s) combination. If environmental conditions detrimentally affect even one component of this symbiotic consortium, it may lead to a cascade effect and the collapse of the entire symbiosis. Symbiosis is at the heart of the coral reef ecosystem, its existence, and its high biodiversity. Climate change may cause the demise of some of the cnidarian symbioses, leading to subsequent reduction in biodiversity on coral reefs.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1016/j.tree.2019.04.010
