Dataset Information

Genome-Wide Analysis of Cell Cycle-Regulating Genes in the Symbiotic Dinoflagellate Breviolum minutum.

ABSTRACT: A delicate relationship exists between reef-building corals and their photosynthetic endosymbionts. Unfortunately, this relationship can be disrupted, with corals expelling these algae when temperatures rise even marginally above the average summer maximum. Interestingly, several studies indicate that failure of corals to regulate symbiont cell divisions at high temperatures may underlie this disruption; increased proliferation of symbionts may stress host cells by over-production of reactive oxygen species or by disrupting the flow of nutrients. This needs to be further investigated, so to begin deciphering the molecular mechanisms controlling the cell cycle in these organisms, we used a computational approach to identify putative cell cycle-regulating genes in the genome of the dinoflagellate Breviolum minutum This species is important as an endosymbiont of Aiptasia pallida-an anemone that is used as a model for studying coral biology. We then correlated expression of these putative cell cycle genes with cell cycle phase in diurnally growing B. minutum in culture. This approach allowed us to identify a cyclin/cyclin-dependent kinase pair that may function in the G1/S transition-a likely point for coral cells to exert control over algal cell divisions.

SUBMITTER: Cato ML

PROVIDER: S-EPMC6829154 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Publications

Genome-Wide Analysis of Cell Cycle-Regulating Genes in the Symbiotic Dinoflagellate <i>Breviolum minutum</i>.

Cato Michael L ML Jester Hallie D HD Lavertu Adam A Lyman Audrey A Tallent Lacey M LM Mitchell Geoffrey C GC

G3 (Bethesda, Md.) 20191105 11

A delicate relationship exists between reef-building corals and their photosynthetic endosymbionts. Unfortunately, this relationship can be disrupted, with corals expelling these algae when temperatures rise even marginally above the average summer maximum. Interestingly, several studies indicate that failure of corals to regulate symbiont cell divisions at high temperatures may underlie this disruption; increased proliferation of symbionts may stress host cells by over-production of reactive ox ...[more]

PMID: 31551286

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Project description:BackgroundDinoflagellates are unicellular marine and freshwater eukaryotes. They possess large nuclear genomes (1.5-245 gigabases) and produce structurally unique and biologically active polyketide secondary metabolites. Although polyketide biosynthesis is well studied in terrestrial and freshwater organisms, only recently have dinoflagellate polyketides been investigated. Transcriptomic analyses have characterized dinoflagellate polyketide synthase genes having single domains. The Genus Symbiodinium, with a comparatively small genome, is a group of major coral symbionts, and the S. minutum nuclear genome has been decoded.ResultsThe present survey investigated the assembled S. minutum genome and identified 25 candidate polyketide synthase (PKS) genes that encode proteins with mono- and multifunctional domains. Predicted proteins retain functionally important amino acids in the catalytic ketosynthase (KS) domain. Molecular phylogenetic analyses of KS domains form a clade in which S. minutum domains cluster within the protist Type I PKS clade with those of other dinoflagellates and other eukaryotes. Single-domain PKS genes are likely expanded in dinoflagellate lineage. Two PKS genes of bacterial origin are found in the S. minutum genome. Interestingly, the largest enzyme is likely expressed as a hybrid non-ribosomal peptide synthetase-polyketide synthase (NRPS-PKS) assembly of 10,601 amino acids, containing NRPS and PKS modules and a thioesterase (TE) domain. We also found intron-rich genes with the minimal set of catalytic domains needed to produce polyketides. Ketosynthase (KS), acyltransferase (AT), and acyl carrier protein (ACP) along with other optional domains are present. Mapping of transcripts to the genome with the dinoflagellate-specific spliced leader sequence, supports expression of multifunctional PKS genes. Metabolite profiling of cultured S. minutum confirmed production of zooxanthellamide D, a polyhydroxy amide polyketide and other unknown polyketide secondary metabolites.ConclusionThis genomic survey demonstrates that S. minutum contains genes with the minimal set of catalytic domains needed to produce polyketides and provides evidence of the modular nature of Type I PKS, unlike monofunctional Type I PKS from other dinoflagellates. In addition, our study suggests that diversification of dinoflagellate PKS genes comprises dinoflagellate-specific PKS genes with single domains, multifunctional PKS genes with KS domains orthologous to those of other protists, and PKS genes of bacterial origin.

Dataset Information

Genome-Wide Analysis of Cell Cycle-Regulating Genes in the Symbiotic Dinoflagellate Breviolum minutum.

Publications

Genome-Wide Analysis of Cell Cycle-Regulating Genes in the Symbiotic Dinoflagellate <i>Breviolum minutum</i>.

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