Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis

Huanle Liu,Timothy G Stephens,Mark A Ragan,Bruno Lapeyre,Madeleine J H Van Oppen,Victor H Beltran,Cheong Xin Chan,Christian R Voolstra,Ira Cooke,David G Bourne,Sylvain Forêt,David J Miller,Raúl A González-Pech,Pim Bongaerts,Manuel Aranda

doi:10.1038/s42003-018-0098-3

Abstract

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.

Highlights

Despite the critical importance of this coral-dinoflagellate symbiosis, little is known about the underlying molecular mechanisms, largely due to the lack of comprehensive understanding of what molecules, pathways and functions Symbiodinium can contribute
Genome-size estimates based on k-mer coverage are 1.19 Gbp for S. goreaui and 1.07 Gbp for S. kawagutii (Supplementary Table 3), comparable to those for other sequenced Symbiodinium genomes
We report fewer genes than in the published Symbiodinium genomes[12,13,14], most (67.0 and 64.4% for S. goreaui and S. kawagutii, respectively) have transcriptome support; and we generally recovered more (Supplementary Fig. 7) of the 458 conserved core eukaryote genes (e.g. 436 in S. goreaui compared to 410 in the published S. microadriaticum[12] based on TBLASTX; Supplementary Fig. 7C)

Summary

Introduction

Despite the critical importance of this coral-dinoflagellate symbiosis, little is known about the underlying molecular mechanisms (apart from photosynthesis and carbon exchange), largely due to the lack of comprehensive understanding of what molecules, pathways and functions Symbiodinium can contribute. We report draft genomes of two Symbiodinium from the Pacific Ocean: Symbiodinium goreaui (type C1; isolated from the acroporid coral Acropora tenuis) from the Great Barrier Reef, and Symbiodinium kawagutii CS-156 (=CCMP2468, Clade F) from Hawaii. Our results indicate adaptive selection in Symbiodinium gene functions that are related to establishment of cnidarian-dinoflagellate symbiosis, and provide compelling genomic evidence (based on gene repertoire) that Symbiodinium is, or has recently been, capable of meiosis. To our knowledge, this is the most comprehensive comparative analysis so far of Symbiodinium genomes, and the first to include a prominent endosymbiont of corals of Indo-Pacific and Caribbean reefs

Methods

Results

Conclusion