Opinion
Genome Evolution of Coral Reef Symbionts as Intracellular Residents

https://doi.org/10.1016/j.tree.2019.04.010Get rights and content

Highlights

  • 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.

Section snippets

Symbiodiniaceae: Critical Symbionts of Coral Reefs

Dinoflagellates of the family Symbiodiniaceae are the most prevalent photosynthetic symbionts in tropical and subtropical coral reef ecosystems. Although dinoflagellates are primarily free-living, Symbiodiniaceae have diversified mainly as symbiotic lineages. Previously classified within the genus Symbiodinium and colloquially known as zooxanthellae, Symbiodiniaceae are associated with diverse hosts including corals, jellyfish, clams, and foraminiferans. These symbiotic interactions can occur

Free-Living Species

At one end of the spectrum, some Symbiodiniaceae species have not been found to be associated with a host. These free-living taxa include some species in the Symbiodinium genus (former Clade A; e.g., the type species S. natans and S. pilosum), the exclusively free-living Effrenium genus (former Clade E), and Fugacium (former Clade F) 2., 4..

A free-living lifestyle presents opportunities for the exchange of genetic material (e.g., recombination via sexual reproduction) with conspecifics,

Facultative Symbionts

Most Symbiodiniaceae are symbiotic, representing a broad spectrum of symbiotic associations and a range of host specificity. Their genomes would have experienced the phase of genome instability during the early transition stages to an intracellular lifestyle (and symbiosis). The genomes during this phase may be larger than those of well-established residents and have accumulated extensive structural rearrangements, mobile elements, and pseudogenes (Figure 1B), as observed in other facultative

Obligate Symbionts

At the other end of the spectrum, some Symbiodiniaceae may be obligate symbionts. These taxa are rarely, if at all, found in the environment or reported in culture. However, one cannot dismiss that brief ex hospite stages may still occur due to regular adjustments of symbiont density by the hosts. In the scenario of strict obligate symbionts (Figure 1C), genomes are expected to follow the evolutionary trajectory postulated in the resident genome syndrome (Box 1).

The effective population size (Ne

Concluding Remarks and Future Perspectives

The recent availability of draft genomes from Symbiodiniaceae and systematic revision of these taxa are allowing investigators to venture deeper into the evolutionary history of these ecologically important organisms. In this Opinion article, we discuss the genome evolution of Symbiodiniaceae across the broad spectrum of symbiotic associations. We acknowledge that Symbiodiniaceae ecology is highly intricate. For instance, host specificity does not always correlate with transmission mode or with

Outstanding Questions

  • How often do Symbiodiniaceae reproduce sexually and under what conditions?

  • How viable are ex hospite cells in distinct symbiotic Symbiodiniaceae taxa?

  • Does the burst of mobile element activity in symbiodiniacean genomes relate to the transition to symbiosis and/or the diversification of these lineages?

  • To what extent do genomes of symbiotic Symbiodiniaceae and other eukaryote residents exhibit symptoms of the resident genome syndrome?

  • Can the accelerated evolutionary rates typical of intracellular

Acknowledgments

R.A.G-P. is supported by an International Postgraduate Research Scholarship and a University of Queensland Centenary Scholarship. This work is supported by Australian Research Council grant DP150101875 awarded to M.A.R., C.X.C., and D.B. and DP190102474 awarded to C.X.C. and D.B.

Glossary

Effective population size (Ne)
in population genetics, the number of effectively reproducing individuals under the assumption of an ideal population.
Genetic drift
evolutionary mechanism in which the changes in allele frequencies of a population are driven by chance.
Genome phasing
statistical estimation of alleles (or haplotypes) from potentially heterozygous genome data.
Horizontal transmission
mode of symbiont transmission in corals in which the dinoflagellate symbionts can be acquired from the

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