Integrated omics unveil the secondary metabolic landscape of a basal dinoflagellate
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RESEARCH ARTICLE
Open Access
Integrated omics unveil the secondary metabolic landscape of a basal dinoflagellate Girish Beedessee1,2* , Takaaki Kubota3, Asuka Arimoto1,4, Koki Nishitsuji1, Ross F. Waller5, Kanako Hisata1, Shinichi Yamasaki6, Noriyuki Satoh1, Jun’ichi Kobayashi7 and Eiichi Shoguchi1
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. Keywords: Polyketide synthases, Harmful algal blooms, Dinoflagellates, Iso-Seq, Duplication, Amphidinium
Background Phytoplankton communities are essential components of marine ecosystems, and dinoflagellates are of special interest because they exhibit morphological diversity, high species richness, and the capacity to survive in different ecological niches [1]. They are also infamous contributors to harmful algal blooms (HABs), often * Correspondence: [email protected] 1 Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan 2 Present address: Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, UK Full list of author information is available at the end of the article
producing toxins that are deadly to aquatic organisms and humans [2]. Dinoflagellates exhibit many genetic and cellular features that are highly unusual for eukaryotes. The persistent condensed state of dinoflagellate chromosomes and their liquid crystalline organization, loss of nucleosomal chromatin packaging, use of 5hydroxymethyluracil in nuclear genomic DNA, and huge
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