Genome Evolution of Coral Reef Symbionts as Intracellular Residents

Coral reefs are sustained by long-term symbiosis between coral animals and dinoflagellate algae of the family Symbiodiniaceae. Genomic studies have shed light on the molecular basis of the coral–dinoflagellate symbiosis. Evolutionary mechanisms that underpin the transition of dinoflagellates in the family Symbiodiniaceae from free-living to symbiotic remain largely unknown. Symbiodiniacean dinoflagellates are expected to share common evolutionary trajectories with other intracellular symbionts and parasites. Comparison of the genome features of Symbiodiniaceae with those of other intracellular residents will improve our understanding of their evolutionary history and of other eukaryote–eukaryote symbioses. 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. 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. in population genetics, the number of effectively reproducing individuals under the assumption of an ideal population. evolutionary mechanism in which the changes in allele frequencies of a population are driven by chance. statistical estimation of alleles (or haplotypes) from potentially heterozygous genome data. mode of symbiont transmission in corals in which the dinoflagellate symbionts can be acquired from the environment. any unicellular organism that has adapted to a lifestyle inside the cell(s) of another organism (host). uptake and establishment of genetic material from one organism to another, instead of vertical parent-to-offspring inheritance. accumulation of nonreversible deleterious mutations in a population as a consequence of asexual reproduction (or lack of recombination); named after the American geneticist Hermann Joseph Muller. type of symbiotic association in which the symbiont lives on or in another organism (the host) such that both the symbiont and the host benefit from interacting with each other. type of symbiotic association in which the symbiont (opportunist) lives on or in another organism (the host) that is experiencing detrimental conditions. technique in which mapped locations of restriction enzyme sites in a genome are used to construct ordered maps to facilitate the determination of distances between and the ordering of DNA fragments in a genome assembly. type of symbiotic association in which the symbiont (parasite) lives on or in another organism (the host) causing the host some loss of fitness. series of genome features shared by intracellular residents, the most remarkable being genome reduction, accelerated evolutionary rates, and mutation bias; originally described for bacteria [7.Andersson S.G. Kurland C.G. Reductive evolution of resident genomes.Trends Microbiol. 1998; 6: 263-268Abstract Full Text Full Text PDF PubMed Scopus (394) Google Scholar, 8.Moran N.A. Wernegreen J.J. Lifestyle evolution in symbiotic bacteria: insights from genomics.Trends Ecol. Evol. 2000; 15: 321-326Abstract Full Text Full Text PDF PubMed Scopus (276) Google Scholar]. co-occurrence of genetic elements in a specified region of a genome. mode of symbiont transmission in corals in which the dinoflagellate symbionts are passed on through coral generations from parents to offspring.