An official website of the United States government
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.
more »
« less
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.
more »
« less
- 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
More Like this
-
-
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
-
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
-
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 voratumand the symbioticSymbiodinium microadriaticumandDurusdinium 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.more » « less
-
Photosynthetic dependence and filament production in physical bacterial–Symbiodiniaceae interactionsAbstract The cnidarian microbiome consists of a wide variety of beneficial microbes that play vital roles in maintaining and fortifying host health. Photosynthesis from symbiotic dinoflagellates (in the family Symbiodiniaceae) is crucial for their symbiosis establishment with the cnidarian host. Although more is known regarding interactions between the host and its associated bacteria and dinoflagellates, there has been little investigation into the relationship between the two microbes themselves and whether photosynthesis plays a role. Through two different methods of photosynthetic inhibition of dinoflagellates (incubation in the dark or pre-treatment with a photosystem II inhibitor), we investigated how pathogenic versus beneficial bacteria physically interact with three Symbiodiniaceae strains (symbiotic and free-living). The beneficial bacterium Tritonibacter mobilis appears to interact with photosynthesizing algae only. In the absence of photosynthesis, little to no physical interactions were observed between Symbiodiniaceae and T. mobilis. Bacterial congregation around individual dinoflagellate cells was significantly lower when photosynthesis was impaired, suggesting photosynthesis is a key facilitator of interactions between T. mobilis and all three Symbiodiniaceae strains. We also investigated whether photosynthesis affects interactions between Symbiodiniaceae and the pathogen Vibrio alginolyticus. Although no discernable impacts of photosynthetic inhibition were observed with the pathogen, scanning electron microscopy uncovered various mechanisms of interaction between Symbiodiniaceae and both bacteria, one of which includes the production of filaments not previously described. Overall, our research highlights the importance of photosynthesis in initiating interactions between bacteria and both free-living and symbiotic dinoflagellates, and opens a door to new questions regarding cell-surface interactions among individual microbes.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1016/j.tree.2019.04.010
