Integrated omics unveil the secondary metabolic landscape of a basal dinoflagellate

Girish Beedessee, Takaaki Kubota, Asuka Arimoto, Koki Nishitsuji, Ross F. Waller, Kanako Hisata, Shinichi Yamasaki, Noriyuki Satoh, Jun’ichi Kobayashi, Eiichi Shoguchi

Research output: Contribution to journalArticlepeer-review

3 Citations (Scopus)

Abstract

Background: Some dinoflagellates cause harmful algal blooms, releasing toxic secondary metabolites, to the detriment of marine ecosystems and human health. Our understanding of dinoflagellate toxin biosynthesis has been hampered by their unusually large genomes. To overcome this challenge, for the first time, we sequenced the genome, microRNAs, and mRNA isoforms of a basal dinoflagellate, Amphidinium gibbosum, and employed an integrated omics approach to understand its secondary metabolite biosynthesis. Results: We assembled the ~ 6.4-Gb A. gibbosum genome, and by probing decoded dinoflagellate genomes and transcriptomes, we identified the non-ribosomal peptide synthetase adenylation domain as essential for generation of specialized metabolites. Upon starving the cells of phosphate and nitrogen, we observed pronounced shifts in metabolite biosynthesis, suggestive of post-transcriptional regulation by microRNAs. Using Iso-Seq and RNA-seq data, we found that alternative splicing and polycistronic expression generate different transcripts for secondary metabolism. Conclusions: Our genomic findings suggest intricate integration of various metabolic enzymes that function iteratively to synthesize metabolites, providing mechanistic insights into how dinoflagellates synthesize secondary metabolites, depending upon nutrient availability. This study provides insights into toxin production associated with dinoflagellate blooms. The genome of this basal dinoflagellate provides important clues about dinoflagellate evolution and overcomes the large genome size, which has been a challenge previously.

Original languageEnglish
Article number139
JournalBMC Biology
Volume18
Issue number1
DOIs
Publication statusPublished - Dec 1 2020
Externally publishedYes

Keywords

  • Amphidinium
  • Dinoflagellates
  • Duplication
  • Harmful algal blooms
  • Iso-Seq
  • Polyketide synthases

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

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