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.2022 Aug 17;10(8):1662.
doi: 10.3390/microorganisms10081662.

ImprovedCladocopium goreaui Genome Assembly Reveals Features of a Facultative Coral Symbiont and the Complex Evolutionary History of Dinoflagellate Genes

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ImprovedCladocopium goreaui Genome Assembly Reveals Features of a Facultative Coral Symbiont and the Complex Evolutionary History of Dinoflagellate Genes

Yibi Chen et al. Microorganisms..

Abstract

Dinoflagellates of the family Symbiodiniaceae are crucial photosymbionts in corals and other marine organisms. Of these,Cladocopium goreaui is one of the most dominant symbiont species in the Indo-Pacific. Here, we present an improved genome assembly ofC. goreaui combining new long-read sequence data with previously generated short-read data. Incorporating new full-length transcripts to guide gene prediction, theC. goreaui genome (1.2 Gb) exhibits a high extent of completeness (82.4% based on BUSCO protein recovery) and better resolution of repetitive sequence regions; 45,322 gene models were predicted, and 327 putative, topologically associated domains of the chromosomes were identified. Comparison with other Symbiodiniaceae genomes revealed a prevalence of repeats and duplicated genes inC. goreaui, and lineage-specific genes indicating functional innovation. Incorporating 2,841,408 protein sequences from 96 taxonomically diverse eukaryotes and representative prokaryotes in a phylogenomic approach, we assessed the evolutionary history ofC. goreaui genes. Of the 5246 phylogenetic trees inferred from homologous protein sets containing two or more phyla, 35-36% have putatively originated via horizontal gene transfer (HGT), predominantly (19-23%) via an ancestral Archaeplastida lineage implicated in the endosymbiotic origin of plastids: 10-11% are of green algal origin, including genes encoding photosynthetic functions. Our results demonstrate the utility of long-read sequence data in resolving structural features of a dinoflagellate genome, and highlight how genetic transfer has shaped genome evolution of a facultative symbiont, and more broadly of dinoflagellates.

Keywords: Cladocopium goreaui; dinoflagellates; genome; horizontal gene transfer; phylogenomics.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Figures

Figure 1
Figure 1
Genome features ofC. goreaui. (a) Repeat families identified in the revised genome assembly; repeat landscape shown for the (b) revised genome assembly ofC. goreaui (highlighted in bold-face) and (c) the earlier assembly of Chen et al. [15]. (d) Frequency of strand-orientation change in 10-gene windows and (e) cumulative percentage of genes in unidirectionally encoded blocks, shown for five representative Symbiodiniaceae genomes:Breviolum minutum [15],C. goreaui [15],C. goreaui (boldfaced, this study),Fugacium kawagutii [19], andSymbiodinium microadriaticum [20]; and (f) number of inter-block regions in each genome assembly indicating putative TAD central regions and boundaries, shown for representative genomes, based on the minimum number of genes in a unidirectional block. Bars above thex-axis represent inter-block regions at which orientations of unidirectional blocks converged, whereas bars below thex-axis represent those at which the orientations diverged.
Figure 2
Figure 2
Evolutionary origins ofC. goreaui genes. (a)C. goreaui genes classified based on the number of recovered protein homologs in other taxa. (b) Distribution of phyla with respect to exclusive gene-sharing partners forC. goreaui, based on the number of homologous sets that contain onlyC. goreaui and the other phylum, across the minimum number of genes in each set (x) atx ≥ 2, ≥ 20, ≥ 40, and ≥ 60. (c) Distribution of phyla that are found to share genes with dinoflagellates, based on the number of inferred protein trees in which dinoflagellates and one other phylum were recovered in a monophyletic clade, assessed at bootstrap support (BS) ≥ 90%, ≥ 70%, and ≥ 50%. All taxonomic classification follows NCBI Taxonomy, including Dinophyceae (Fritsch 1927).
Figure 3
Figure 3
Maximum likelihood trees of (a) beta-glucan synthesis-associated protein and (b) abscisic acid 8′-hydroxylase, suggesting ancient gene origins from Viridiplantae. The ultrafast bootstrap support of IQ-TREE2 is shown at each internal node; only values ≥ 70% are shown. Unit of branch length is the number of substitutions per site.
Figure 4
Figure 4
Maximum likelihood tree of putative sulphate transporter indicating a Viridiplantae origin in dinoflagellate genes. The ultrafast bootstrap support of IQ-TREE2 is shown at each internal node; only values ≥ 70% are shown. Unit of branch length is the number of substitutions per site.
Figure 5
Figure 5
Maximum likelihood protein tree showing vertical inheritance and gene expansion among dinoflagellates, with distinct clades containing the autophagy-related protein 18a, the transmembrane protein 43, and the pentatricopeptide repeat-containing protein GUN1. The ultrafast bootstrap support of IQ-TREE2 is shown at each internal node; only values ≥ 70% are shown. Unit of branch length is the number of substitutions per site.
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