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

Type Article
Date 2020-04
Language English
Author(s) Van Dolah Frances M.1, 4, Morey Jeanine S.1, 5, Milne Shard2, 6, Ung Andre3, Anderson Paul E.2, 7, Chinain Mireille3
Affiliation(s) 1 : Hollings Marine Lab, Marine Genom Core, Charleston, SC 29412 USA.
2 : Coll Charleston, Dept Comp Sci, Charleston Computat Genom Grp, Charleston, SC 29401 USA.
3 : Inst Louis Malarde UMR 241 EIO, Lab Biotoxines Marines, Tahiti, French Polynesi, France.
4 : Univ Charleston, Grad Program Marine Biol, Charleston, SC 29424 USA.
5 : Natl Marine Mammal Fdn, Johns Isl, SC USA.
6 : Univ Washington, Sch Environm & Forest Sci, Seattle, WA 98195 USA.
7 : Calif Polytech State Univ San Luis Obispo, Dept Comp Sci & Software Engn, San Luis Obispo, CA 93407 USA.
Source Plos One (1932-6203) (Public Library Science), 2020-04 , Vol. 15 , N. 4 , P. e0231400 (21p.)
DOI 10.1371/journal.pone.0231400
WOS© Times Cited 4
Abstract Marine dinoflagellates produce a diversity of polyketide toxins that are accumulated in marine food webs and are responsible for a variety of seafood poisonings. Reef-associated dinoflagellates of the genus Gambierdiscus produce toxins responsible for ciguatera poisoning (CP), which causes over 50,000 cases of illness annually worldwide. The biosynthetic machinery for dinoflagellate polyketides remains poorly understood. Recent transcriptomic and genomic sequencing projects have revealed the presence of Type I modular polyketide synthases in dinoflagellates, as well as a plethora of single domain transcripts with Type I sequence homology. The current transcriptome analysis compares polyketide synthase (PKS) gene transcripts expressed in two species of Gambierdiscus from French Polynesia: a highly toxic ciguatoxin producer, G. polynesiensis, versus a non-ciguatoxic species G. pacificus, each assembled from approximately 180 million Illumina 125 nt reads using Trinity, and compares their PKS content with previously published data from other Gambierdiscus species and more distantly related dinoflagellates. Both modular and single-domain PKS transcripts were present. Single domain beta-ketoacyl synthase (KS) transcripts were highly amplified in both species (98 in G. polynesiensis, 99 in G. pacificus), with smaller numbers of standalone acyl transferase (AT), ketoacyl reductase (KR), dehydratase (DH), enoyl reductase (ER), and thioesterase (TE) domains. G. polynesiensis expressed both a larger number of multidomain PKSs, and larger numbers of modules per transcript, than the non-ciguatoxic G. pacificus. The largest PKS transcript in G. polynesiensis encoded a 10,516 aa, 7 module protein, predicted to synthesize part of the polyether backbone. Transcripts and gene models representing portions of this PKS are present in other species, suggesting that its function may be performed in those species by multiple interacting proteins. This study contributes to the building consensus that dinoflagellates utilize a combination of Type I modular and single domain PKS proteins, in an as yet undefined manner, to synthesize polyketides.
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Publisher's official version 21 1 MB Open access
S1 Fig. Single domain KS homologs present in G. polynesiensis and G. pacificus identified by phylogenetic analysis. 758 KB Open access
S2 Fig. Maximum likelihood analysis of TE Domains in G. polynesiensis and G. pacificus. 148 KB Open access
S1 Table. Deeploc intracellular localization assignment of G. polynesiensis single domain KS. 21 KB Open access
S2 Table. Deeploc intracellular localization assignment of G. pacificus single domain KS. 16 KB Open access
S3 Table. Deeploc intracellular localization assignment of G. polynesiensis single domain KS. 20 KB Open access
S4 Table. Deeploc intracellular localization assignment of G. pacificus single domain KS. 19 KB Open access
S5 Table. Genbank accession numbers for peroxisomal proteins identified in G. polynesiensis TB92 and G. pacificus MUR4. 11 KB Open access
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Van Dolah Frances M., Morey Jeanine S., Milne Shard, Ung Andre, Anderson Paul E., Chinain Mireille (2020). Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia. Plos One, 15(4), e0231400 (21p.). Publisher's official version : https://doi.org/10.1371/journal.pone.0231400 , Open Access version : https://archimer.ifremer.fr/doc/00657/76863/