Structural rearrangements drive extensive genome divergence between symbiotic and free-living Symbiodinium

Abstract

16Symbiodiniaceae are predominantly symbiotic dinoflagellates critical to corals and other reef 17 organisms. Symbiodinium is a basal symbiodiniacean lineage and includes symbiotic and free-living 18 taxa. However, the molecular mechanisms underpinning these distinct lifestyles remain little 19 known. Here, we present high-quality de novo genome assemblies for the symbiotic Symbiodinium 20 tridacnidorum CCMP2592 (genome size 1.3 Gbp) and the free-living Symbiodinium natans 21 CCMP2548 (genome size 0.74 Gbp). These genomes display extensive sequence divergence, 22sharing only ~1.5% conserved regions (≥90% identity). We predicted 45,474 and 35,270 genes for 23 S. tridacnidorum and S. natans, respectively; of the 58,541 homologous gene families, 28.5% are 24 common to both genomes. We recovered a greater extent of gene duplication and higher abundance 25 of repeats, transposable elements and pseudogenes in the genome of S. tridacnidorum than in that of 26 S. natans. These findings demonstrate that genome structural rearrangements are pertinent to 27 distinct lifestyles in Symbiodinium, and may contribute to the vast genetic diversity within the 28 genus, and more broadly in Symbiodiniaceae. Moreover, the results from our whole-genome 29 comparisons against a free-living outgroup support the notion that the symbiotic lifestyle is a 30 derived trait in, and that the free-living lifestyle is ancestral to, Symbiodinium. 31 with the potential to shift between a free-living motile stage (i.e. mastigote form) and a spherical 56 symbiotic stage (i.e. coccoid form). The genomes of facultative and recent intracellular symbionts 57 and parasites are usually very unstable, with extensive structural rearrangements, intensified activity 58 of transposable elements (TEs) and exacerbated gene duplication that leads to the accumulation of 59 pseudogenes 19,20 . Symbiotic Symbiodiniaceae are thus expected to display similar genomic features. 60In this study, we present draft de novo genome assemblies of S. tridacnidorum CCMP2592 and S. 61 natans CCMP2548. Using a comparative genomic approach, we found extensive genome-sequence 62 divergence and few shared families of predicted genes between the two species. A greater extent of 63 gene duplication, and the higher abundance of TEs and pseudogenes in S. tridacnidorum relative to 64 S. natans suggest that duplication and transposition underpin genome divergence between these 65 species. 66 5

Genomes of Symbiodiniaceae reveal extensive sequence divergence but conserved functions at family and genus levels

“…For a comprehensive comparison, we included in our analysis all available genome data from Symbiodiniaceae and the outgroup species of Polarella glacialis (Supplementary Table 1). These data comprise nine Symbiodinium isolates (three of the species S. microadriaticum and two of S. tridacnidorum ), Breviolum minutum , two Cladocopium isolates, Fugacium kawagutii , and two Polarella glacialis isolates 8,10–14 ( i.e. a total of 15 datasets of Suessiales, of which 13 are of Symbiodiniaceae); we used the revised genome assemblies from Chen et al 15 where applicable.…”

“…a total of 15 datasets of Suessiales, of which 13 are of Symbiodiniaceae); we used the revised genome assemblies from Chen et al 15 where applicable. Of the 15 genome assemblies, four were generated using both short- and long-read data (those of S. natans CCMP2548, S. tridacnidorum CCMP2592 and the two P. glacialis isolates) 8,14 ; all others were generated largely using short-read data.…”

“…The repeat composition of P. glacialis is distinct from that of Symbiodiniaceae genomes, largely due to the known prevalence of simple repeats 8,14 . Long interspersed nuclear elements (LINEs) in Symbiodiniaceae and in P. glacialis are highly diverged, with Kimura distance centred between 15 and 40; these elements likely represent remnants of LINEs from an ancient burst pre-dating the diversification of Suessiales 8,11,14 . Interestingly, the proportion of these elements is substantially larger in the genomes of Symbiodinium (the basal lineage) and P. glacialis (the outgroup) than in those of other Symbiodiniaceae (Fig.…”

“…Among the core genes of Symbiodiniaceae, the most significantly overrepresented GO terms relate to retrotransposition, components of the membrane (including ABC transporters), cellulose binding, and reduction and oxidation reactions of the electron transport chain (Supplementary Table 5). Retrotransposition has been shown to contribute to gene-family expansion and changes in the gene structure of Symbiodiniaceae 8,18 . The enrichment of this function in Symbiodiniaceae may be due to a common origin of genes that encode remnant protein domains from past retrotransposition events ( e.g.…”

“…An earlier comparative study using predicted genes from available transcriptome and genome data revealed that functions pertinent to symbiosis are common to all Symbiodiniaceae, but the differences in gene-family number among the major lineages are possibly associated with adaptation to more-specialised ecological niches 7 . A recent investigation 8 revealed little similarity between the whole-genome sequences of a symbiotic and a free-living Symbiodinium species. However, whether this sequence divergence is an isolated case, or is associated with the distinct lifestyles, remains to be investigated using more genome-scale data.…”