Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates

Jeremiah D. Hackett, Jennifer H. Wisecaver, Michael L. Brosnahan, David M. Kulis, Donald M. Anderson, Debashish Bhattacharya, F. Gerald Plumley, Deana L. Erdner

Research output: Contribution to journalArticle

92 Scopus citations

Abstract

Dinoflagellates produce a variety of toxic secondary metabolites that have a significant impact on marine ecosystems and fisheries. Saxitoxin (STX), the cause of paralytic shellfish poisoning, is produced by three marine dinoflagellate genera and is also made by some freshwater cyanobacteria. Genes involved in STX synthesis have been identified in cyanobacteria but are yet to be reported in the massive genomes of dinoflagellates. We have assembled comprehensive transcriptome data sets for several STX-producing dinoflagellates and a related non-toxic species and have identified 265 putative homologs of 13 cyanobacterial STX synthesis genes, including all of the genes directly involved in toxin synthesis. Putative homologs of four proteins group closely in phylogenies with cyanobacteria and are likely the functional homologs of sxtA, sxtG, and sxtB in dinoflagellates. However, the phylogenies do not support the transfer of these genes directly between toxic cyanobacteria and dinoflagellates. SxtA is split into two proteins in the dinoflagellates corresponding to the N-terminal portion containing the methyltransferase and acyl carrier protein domains and a C-terminal portion with the aminotransferase domain. Homologs of sxtB and N-terminal sxtA are present in non-toxic strains, suggesting their functions may not be limited to saxitoxin production. Only homologs of the C-terminus of sxtA and sxtG were found exclusively in toxic strains. A more thorough survey of STX+ dinoflagellates will be needed to determine if these two genes may be specific to SXT production in dinoflagellates. The A. tamarense transcriptome does not contain homologs for the remaining STX genes. Nevertheless, we identified candidate genes with similar predicted biochemical activities that account for the missing functions. These results suggest that the STX synthesis pathway was likely assembled independently in the distantly related cyanobacteria and dinoflagellates, although using some evolutionarily related proteins. The biological role of STX is not well understood in either cyanobacteria or dinoflagellates. However, STX production in these two ecologically distinct groups of organisms suggests that this toxin confers a benefit to producers that we do not yet fully understand.

Original languageEnglish (US)
Pages (from-to)70-78
Number of pages9
JournalMolecular biology and evolution
Volume30
Issue number1
DOIs
StatePublished - Jan 2013

Keywords

  • Saxitoxin
  • dinoflagellate
  • evolution
  • gene transfer
  • secondary metabolism
  • toxin

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

Fingerprint Dive into the research topics of 'Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates'. Together they form a unique fingerprint.

  • Cite this

    Hackett, J. D., Wisecaver, J. H., Brosnahan, M. L., Kulis, D. M., Anderson, D. M., Bhattacharya, D., Gerald Plumley, F., & Erdner, D. L. (2013). Evolution of saxitoxin synthesis in cyanobacteria and dinoflagellates. Molecular biology and evolution, 30(1), 70-78. https://doi.org/10.1093/molbev/mss142