Abstract
BackgroundMarine microbial protists, in particular, dinoflagellates, produce polyketide toxins with ecosystem-wide and human health impacts. Species of Gambierdiscus produce the polyether ladder compounds ciguatoxins and maitotoxins, which can lead to ciguatera fish poisoning, a serious human illness associated with reef fish consumption. Genes associated with the biosynthesis of polyether ladder compounds are yet to be elucidated, however, stable isotope feeding studies of such compounds consistently support their polyketide origin indicating that polyketide synthases are involved in their biosynthesis.ResultsHere, we report the toxicity, genome size, gene content and transcriptome of Gambierdiscus australes and G. belizeanus. G. australes produced maitotoxin-1 and maitotoxin-3, while G. belizeanus produced maitotoxin-3, for which cell extracts were toxic to mice by IP injection (LD50 = 3.8 mg kg-1). The gene catalogues comprised 83,353 and 84,870 unique contigs, with genome sizes of 32.5 ± 3.7 Gbp and 35 ± 0.88 Gbp, respectively, and are amongst the most comprehensive yet reported from a dinoflagellate. We found three hundred and six genes involved in polyketide biosynthesis, including one hundred and ninty-two ketoacyl synthase transcripts, which formed five unique phylogenetic clusters.ConclusionsTwo clusters were unique to these maitotoxin-producing dinoflagellate species, suggesting that they may be associated with maitotoxin biosynthesis. This work represents a significant step forward in our understanding of the genetic basis of polyketide production in dinoflagellates, in particular, species responsible for ciguatera fish poisoning.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1625-y) contains supplementary material, which is available to authorized users.
Highlights
Marine microbial protists, in particular, dinoflagellates, produce polyketide toxins with ecosystem-wide and human health impacts
Similar to the proposed biosynthetic pathway for BTXs [7, 14], we propose a possible biosynthetic pathway for MTX-1 synthesis (Fig. 1), in which the carbon backbone is synthesised via polyketide biosynthesis followed by epoxidation, polyepoxide cyclisation and sulphonation carried out by polyketide synthases (PKS), epoxidases, epoxide hydrolases and sulfotransferases
Genome size analysis We determined a DNA content of 33.2 ± 3.8 pg cell-1 for Gambierdiscus australes and 35.8 ± 0.9 pg cell-1 for G. belizeanus via flow cytometry (Supplemental data), which equates to a genome size of 32.5 ± 3.7 Gbp and 35 ± 0.88 Gbp, respectively (Fig. 2)
Summary
We report the toxicity, genome size, gene content and transcriptome of Gambierdiscus australes and G. belizeanus. G. australes produced maitotoxin-1 and maitotoxin-3, while G. belizeanus produced maitotoxin-3, for which cell extracts were toxic to mice by IP injection (LD50 = 3.8 mg kg-1). The gene catalogues comprised 83,353 and 84,870 unique contigs, with genome sizes of 32.5 ± 3.7 Gbp and 35 ± 0.88 Gbp, respectively, and are amongst the most comprehensive yet reported from a dinoflagellate. We found three hundred and six genes involved in polyketide biosynthesis, including one hundred and ninty-two ketoacyl synthase transcripts, which formed five unique phylogenetic clusters
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