Cargando…
Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia
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 50,0...
Autores principales: | , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2020
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7159223/ https://www.ncbi.nlm.nih.gov/pubmed/32294110 http://dx.doi.org/10.1371/journal.pone.0231400 |
_version_ | 1783522619704737792 |
---|---|
author | Van Dolah, Frances M. Morey, Jeanine S. Milne, Shard Ung, André Anderson, Paul E. Chinain, Mireille |
author_facet | Van Dolah, Frances M. Morey, Jeanine S. Milne, Shard Ung, André Anderson, Paul E. Chinain, Mireille |
author_sort | Van Dolah, Frances M. |
collection | PubMed |
description | 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 β-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. |
format | Online Article Text |
id | pubmed-7159223 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-71592232020-04-22 Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia Van Dolah, Frances M. Morey, Jeanine S. Milne, Shard Ung, André Anderson, Paul E. Chinain, Mireille PLoS One Research Article 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 β-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. Public Library of Science 2020-04-15 /pmc/articles/PMC7159223/ /pubmed/32294110 http://dx.doi.org/10.1371/journal.pone.0231400 Text en © 2020 Van Dolah et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Van Dolah, Frances M. Morey, Jeanine S. Milne, Shard Ung, André Anderson, Paul E. Chinain, Mireille Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia |
title | Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia |
title_full | Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia |
title_fullStr | Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia |
title_full_unstemmed | Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia |
title_short | Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia |
title_sort | transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, gambierdiscus polynesiensis and low toxicity gambierdiscus pacificus, from french polynesia |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7159223/ https://www.ncbi.nlm.nih.gov/pubmed/32294110 http://dx.doi.org/10.1371/journal.pone.0231400 |
work_keys_str_mv | AT vandolahfrancesm transcriptomicanalysisofpolyketidesynthasesinahighlyciguatoxicdinoflagellategambierdiscuspolynesiensisandlowtoxicitygambierdiscuspacificusfromfrenchpolynesia AT moreyjeanines transcriptomicanalysisofpolyketidesynthasesinahighlyciguatoxicdinoflagellategambierdiscuspolynesiensisandlowtoxicitygambierdiscuspacificusfromfrenchpolynesia AT milneshard transcriptomicanalysisofpolyketidesynthasesinahighlyciguatoxicdinoflagellategambierdiscuspolynesiensisandlowtoxicitygambierdiscuspacificusfromfrenchpolynesia AT ungandre transcriptomicanalysisofpolyketidesynthasesinahighlyciguatoxicdinoflagellategambierdiscuspolynesiensisandlowtoxicitygambierdiscuspacificusfromfrenchpolynesia AT andersonpaule transcriptomicanalysisofpolyketidesynthasesinahighlyciguatoxicdinoflagellategambierdiscuspolynesiensisandlowtoxicitygambierdiscuspacificusfromfrenchpolynesia AT chinainmireille transcriptomicanalysisofpolyketidesynthasesinahighlyciguatoxicdinoflagellategambierdiscuspolynesiensisandlowtoxicitygambierdiscuspacificusfromfrenchpolynesia |