The Genetic Basis of Toxin Biosynthesis in Dinoflagellates

Abstract

In marine ecosystems, dinoflagellates can become highly abundant and even dominant at times, despite their comparatively slow growth rates. One factor that may play a role in their ecological success is the production of complex secondary metabolite compounds that can have anti-predator, allelopathic, or other toxic effects on marine organisms, and also cause seafood poisoning in humans. Our knowledge about the genes involved in toxin biosynthesis in dinoflagellates is currently limited due to the complex genomic features of these organisms. Most recently, the sequencing of dinoflagellate transcriptomes has provided us with valuable insights into the biosynthesis of polyketide and alkaloid-based toxin molecules in dinoflagellate species. This review synthesizes the recent progress that has been made in understanding the evolution, biosynthetic pathways, and gene regulation in dinoflagellates with the aid of transcriptomic and other molecular genetic tools, and provides a pathway for future studies of dinoflagellates in this exciting omics era.

Keywords: alkaloids; dinoflagellates; polyketides; toxins; transcriptomics.

Figure 1

Functional role of toxins produced by dinoflagellates. Schematic representing various biological roles played by toxins for their producing organisms. Photo credit: Diana Kleine, Dieter Tracey, Ian Hewson, Jane Hawkey, Jane Thomas and Tracey Saxby, Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/imagelibrary/).

Figure 2

Polyketide biosynthesis. Schematic representing the putative biosynthesis pathway of polyketide compound Amphidinol-9 by various modular PKS domains represented by ACP: acyl carrier protein, AT: acyl transferase, DH: dehydratase, KR: ketoreductase, and KS: ketosynthase. Figure credit: Gurjeet Singh Kohli.

Figure 3

Ketoacyl synthase (KS) domain phylogeny in dinoflagellates (modified from [81,122,129]). Phylogenetic tree representing the three sub-clades of KS domains within the dinoflagellate type I PKSs, multi-domain PKSs that cluster with other apicomplexans (condensed clade represented by 1), chlorophytes, haptophytes (condensed clade represented by 2) and the burA like PKS-NRPSs reported from dinoflagellates along with schematic representations of PKS domains represented by AT: acyl transferase, A: Non-Ribosomal Peptide Synthase, KS: ketosynthase, DH: dehydratase, KR: ketoreductase, TE: thioesterase, ACP: acyl carrier protein, ER: enoyl reductase, SL: 5’ splice leader, polyA: poly A tail. Other PKS groups are represented by 3: Modular type PKS cis AT clade, 4: fungal PKS non-reducing clade, 5: Animal type I FAS, 6: fugal PKS reducing; and 7: Type II PKSs.

Figure 4

Survey of ketosynthase (KS) domains from various marine microbial eukaryotic lineages (modified from [81]). The figure represents the large number of KS domains that have been reported from the analysis of MMETSP libraries of different dinoflagellate species in comparison with species of cryptophytes, haptophytes, viriplantae, ciliates, diatoms, and other strameopiles. Photo credit: Diana Kleine, Jane Thomas and Tracey Saxby, Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/imagelibrary/).

Figure 5

Revised biosynthetic pathway of PSTs in dinoflagellates (modified from [22,184,185,193,195]). The reaction steps are as follows; 1: Claisen condensation; 2: amidino transfer; 3: heterocyclization; 4: desaturation (Double bond formation); 5: epoxidation of the new double bond; 6: aldehyde formation; 7: terminal aldehyde reduction; 8: dihydroxylation and 9: carbamoylation.

Figure 6

The structure of sxtA and sxtG in dinoflagellates (modified from [57,191]). A. Transcript structure of sxtA short isoform. B. Transcript structure of sxtA long isoform. C. Transcript structure of sxtG. D. Genomic structure of sxtG.