Multimodular type I polyketide synthases in algae evolve by module duplications and displacement of AT domains in trans

Abstract

BackgroundPolyketide synthase (PKS) catalyzes the biosynthesis of polyketides, which are structurally and functionally diverse natural products in microorganisms and plants. Here, we have analyzed available full genome sequences of microscopic and macroscopic algae for the presence of type I PKS genes.ResultsType I PKS genes are present in 15 of 32 analyzed algal species. In chlorophytes, large proteins in the MDa range are predicted in most sequenced species, and PKSs with free-standing acyltransferase domains (trans-AT PKSs) predominate. In a phylogenetic tree, PKS sequences from different algal phyla form clades that are distinct from PKSs from other organisms such as non-photosynthetic protists or cyanobacteria. However, intermixing is observed in some cases, for example polyunsaturated fatty acid (PUFA) and glycolipid synthases of various origins. Close relationships between type I PKS modules from different species or between modules within the same multimodular enzyme were identified, suggesting module duplications during evolution of algal PKSs. In contrast to type I PKSs, nonribosomal peptide synthetases (NRPSs) are relatively rare in algae (occurrence in 7 of 32 species).ConclusionsOur phylogenetic analysis of type I PKSs in algae supports an evolutionary scenario whereby integrated AT domains were displaced to yield trans-AT PKSs. Together with module duplications, the displacement of AT domains may constitute a major mechanism of PKS evolution in algae. This study advances our understanding of the diversity of eukaryotic PKSs and their evolutionary trajectories.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2222-9) contains supplementary material, which is available to authorized users.

Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia

“…The modular PKS contigs identified in G. polynesiensis and G. pacificus were predominantly of trans-AT architecture (Table 3), as previously observed in dinoflagellates [26,27,29] as well as other eukaryotic microalgae [62]. KS domains from cis-AT architectures were mainly associated with hybrid NRPS/PKS.…”

“…Two of three dinoflagellate sub-clades within the cis-AT were NRPS/PKS sequences. The first, with the domain structure TE-A-PP-KS-AT-TE-KR-PP, had similarity to the bacterial Burkholderia burA, previously described in a wide variety of dinoflagellates [32,62]. Contigs containing burA-like full or partial domain arrangements were present in all Gambierdiscus transcriptomes.…”

Both modular and single‐domain Type I polyketide synthases are expressed in the brevetoxin‐producing dinoflagellate, Karenia brevis (Dinophyceae)

“…Trans‐AT PKS architectures were prevalent, as recently reported in PKSs from other eukaryotic microalgae (Shelest et al. ). The longest PKS found in this study consisted of three modules, insufficient by itself to synthesize any of polyethers known to be produced by K. brevis .…”

“…Trans‐AT PKSs have been found to be common among other microalgal PKSs (Shelest et al. ). In the phylogenetic analysis of K. brevis KS domains, most of the multidomain KSs fall within a clade that includes apicomplexan PKSs (Fig.…”

Mining Natural Product Biosynthesis in Eukaryotic Algae

“…Sequencing of algal genomes reveals that many encode natural product biosynthetic genes similar to those encoded by well-studied bacteria and fungi [10]. Many species harbour some polyketide synthases (PKSs), mostly of the trans-acyltransferase type, but there are very few non-ribosomal peptide synthetases (NRPSs) described in algae [11].…”