A New Dinoflagellate Genome Illuminates a Conserved Gene Cluster Involved in Sunscreen Biosynthesis

Abstract

Photosynthetic dinoflagellates of the Family Symbiodiniaceae live symbiotically with many organisms that inhabit coral reefs and are currently classified into fifteen groups, including seven genera. Draft genomes from four genera, Symbiodinium, Breviolum, Fugacium, and Cladocopium, which have been isolated from corals, have been reported. However, no genome is available from the genus Durusdinium, which occupies an intermediate phylogenetic position in the Family Symbiodiniaceae and is well known for thermal tolerance (resistance to bleaching). We sequenced, assembled, and annotated the genome of Durusdinium trenchii, isolated from the coral, Favia speciosa, in Okinawa, Japan. Assembled short reads amounted to 670 Mbp with ∼47% GC content. This GC content was intermediate among taxa belonging to the Symbiodiniaceae. Approximately 30,000 protein-coding genes were predicted in the D. trenchii genome, fewer than in other genomes from the Symbiodiniaceae. However, annotations revealed that the D. trenchii genome encodes a cluster of genes for synthesis of mycosporine-like amino acids (MAAs), which absorb UV radiation. Interestingly, a neighboring gene in the cluster encodes a GMC (glucose-methanol-choline) oxidoreductase with an FAD (flavin adenine dinucleotide) domain that is also found in Symbiodinium tridacnidorum. This conservation seems to partially clarify an ancestral genomic structure in the Symbiodiniaceae and its loss in late-branching lineages, including Breviolum and Cladocopium, after splitting from the Durusdinium lineage. Our analysis suggests that approximately half of the taxa in the Symbiodiniaceae may maintain the ability to synthesize MAAs. Thus, this work provides a significant genomic resource for understanding the genomic diversity of Symbiodiniaceae in corals.

Gene clusters for biosynthesis of mycosporine‐like amino acids in dinoflagellate nuclear genomes: Possible recent horizontal gene transfer between species of Symbiodiniaceae (Dinophyceae)

“…On the other hand, the draft assembly of Durusdinium trenchii , which occupies an intermediate phylogenetic position, contains a gene cluster for MAA biosynthesis, expression of which is supported by transcriptomic data (Shoguchi et al. 2021; Fig. 2b).…”

“…2013, Shoguchi et al. 2021; https://marinegenomics.oist.jp/symbd/viewer/info?project_id=102). Gene structures with exons (blue boxes), introns (black lines) and directions (arrows) are shown on the upper side.…”

Mining genomes to illuminate the specialized chemistry of life

“…Still, even in plants, bGCs are an attractive target for pathway discovery, as they provide 'low-hanging fruits' that can be straightforwardly identified in genome sequences 5 . In protists, several examples of bGCs have been reported 92,225 , whereas not much is known about gene clustering in animals. Yet a recent global synteny network analysis shows that the gene order in mammals is clearly non-random and may have large functional repercussions 226 .…”

Gene Family Complexity and Expression Divergence as a Mechanism of Adaptation In Coral

“…To filter out symbiont transcripts we utilized a previously described approach to symbiont filtration (Sarah W. Davies, Marchetti, Ries, & Castillo, 2016). In short, multiple coral assemblies (Davies, Marchetti, Ries, & Castillo, 2016;Kirk, Howells, Abrego, Burt, & Meyer, 2017;Moya et al, 2012;van de Water et al, 2018 ) were combined to create a coral database, while assemblies from multiple genera of symbionts (Aranda et al, 2016;Liu et al, 2018;Parkinson et al, 2016;Shoguchi et al, 2021) were combined to create a symbiont database. Transcripts from each of our coral assemblies were then queried using blastn against each database and a transcript was retained only if it had greater than 80% identity over at least 100bp to the coral database and that transcript did not have a lower evalue when blasted against the symbiont database.…”

“…In order to determine which genes demonstrate species-specific expression shifts we mapped reads from each coral colony to a holobiont transcriptome with the read mapping program salmon (Patro, Duggal, Love, Irizarry, & Kingsford, 2017) using an index size of 31 in each species. The holobiont transcriptome was generated by combining the host transcripts with available transcriptomes from representatives of four genera of Symbiodiniaceae: Symbiodinium microadriaticum (Aranda et al, 2016), Breviolum minutum (Parkinson et al, 2016), Cladocopium goreaui (Liu et al, 2018), Durusdinium trenchii, (Shoguchi et al, 2021).…”