TY - JOUR
T1 - Integrated omics unveil the secondary metabolic landscape of a basal dinoflagellate
AU - Beedessee, Girish
AU - Kubota, Takaaki
AU - Arimoto, Asuka
AU - Nishitsuji, Koki
AU - Waller, Ross F.
AU - Hisata, Kanako
AU - Yamasaki, Shinichi
AU - Satoh, Noriyuki
AU - Kobayashi, Jun’ichi
AU - Shoguchi, Eiichi
N1 - Funding Information:
GB was supported by a Japanese Society for the Promotion of Science (JSPS) Research Fellowship for Young Scientists and a JSPS Grant-in-Aid for Fellows (17J00597). This work was supported by generous funding from Okinawa Institute of Science and Technology (OIST) Graduate University to the Marine Genomics Unit.
Publisher Copyright:
© 2020, The Author(s).
PY - 2020/12/1
Y1 - 2020/12/1
N2 - 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.
AB - 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.
KW - Amphidinium
KW - Dinoflagellates
KW - Duplication
KW - Harmful algal blooms
KW - Iso-Seq
KW - Polyketide synthases
UR - http://www.scopus.com/inward/record.url?scp=85092774019&partnerID=8YFLogxK
U2 - 10.1186/s12915-020-00873-6
DO - 10.1186/s12915-020-00873-6
M3 - Article
C2 - 33050904
AN - SCOPUS:85092774019
SN - 1741-7007
VL - 18
JO - BMC Biology
JF - BMC Biology
IS - 1
M1 - 139
ER -