Abstract
Symbiodiniaceae dinoflagellates possess smaller nuclear genomes than other dinoflagellates and produce structurally specialized, biologically active, secondary metabolites. Till date, little is known about the evolution of secondary metabolism in dinoflagellates as comparative genomic approaches have been hampered by their large genome sizes. Here, we overcome this challenge by combining genomic and metabolomics approaches to investigate how chemical diversity arises in three decoded Symbiodiniaceae genomes (clades A3, B1 and C). Our analyses identify extensive diversification of polyketide synthase and non-ribosomal peptide synthetase genes from two newly decoded genomes of Symbiodinium tridacnidorum (A3) and Cladocopium sp. (C). Phylogenetic analyses indicate that almost all the gene families are derived from lineage-specific gene duplications in all three clades, suggesting divergence for environmental adaptation. Few metabolic pathways are conserved among the three clades and we detect metabolic similarity only in the recently diverged clades, B1 and C. We establish that secondary metabolism protein architecture guides substrate specificity and that gene duplication and domain shuffling have resulted in diversification of secondary metabolism genes.
Highlights
IntroductionDinoflagellates of the family Symbiodiniaceae[1] (previously known as the genus Symbiodinium) exist freely in symbiotic associations with many invertebrates, such as corals, clams, and anemones
Dinoflagellates of the family Symbiodiniaceae[1] exist freely in symbiotic associations with many invertebrates, such as corals, clams, and anemones
Scanning the GC profile of polyketide synthase (PKS)-I group scaffolds of clade C showed some regions of higher GC content (45–46.5%), compared to the average genomic GC content of 43.0%, indicative of gene transfer (Supplemental Information, Fig. S3). ~3% (3/83) of the sequences contain the cTP signal while 12% (10/83) contained mitochondrial targeting peptide or secretory signal each (Fig. 1)
Summary
Dinoflagellates of the family Symbiodiniaceae[1] (previously known as the genus Symbiodinium) exist freely in symbiotic associations with many invertebrates, such as corals, clams, and anemones This invertebrateSymbiodiniaceae mutualism seems to provide a competitive advantage[2], resulting in the production and exchange of metabolites by both organisms[3]. The Symbiodiniaceae SCCs are polyketide metabolites, that are biosynthesized via an assembly line mechanism by two important classes of modular enzymes, polyketide synthase (PKS) and non-ribosomal peptide synthase (NRPS)[5]. Metabolic pathways accept many different substrates, generating diverse chemical products and this provides organisms with unique chemistry to face environmental challenges[22]. (a.k.a clade C) that produce different metabolites, and surveyed their genomes[17,20] for genes involved in polyketide and non-ribosomal peptide biosynthesis. We examined how these genomes are equipped to expand their gene repertoire for biosynthesis of complex secondary metabolites and suggest possible diversification mechanisms that may contribute to such chemical variability and modularity
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