Horizontal gene transfer is a significant driver of gene innovation in dinoflagellates

Abstract

The dinoflagellates are an evolutionarily and ecologically important group of microbial eukaryotes. Previous work suggests that horizontal gene transfer (HGT) is an important source of gene innovation in these organisms. However, dinoflagellate genomes are notoriously large and complex, making genomic investigation of this phenomenon impractical with currently available sequencing technology. Fortunately, de novo transcriptome sequencing and assembly provides an alternative approach for investigating HGT. We sequenced the transcriptome of the dinoflagellate Alexandrium tamarense Group IV to investigate how HGT has contributed to gene innovation in this group. Our comprehensive A. tamarense Group IV gene set was compared with those of 16 other eukaryotic genomes. Ancestral gene content reconstruction of ortholog groups shows that A. tamarense Group IV has the largest number of gene families gained (314-1,563 depending on inference method) relative to all other organisms in the analysis (0-782). Phylogenomic analysis indicates that genes horizontally acquired from bacteria are a significant proportion of this gene influx, as are genes transferred from other eukaryotes either through HGT or endosymbiosis. The dinoflagellates also display curious cases of gene loss associated with mitochondrial metabolism including the entire Complex I of oxidative phosphorylation. Some of these missing genes have been functionally replaced by bacterial and eukaryotic xenologs. The transcriptome of A. tamarense Group IV lends strong support to a growing body of evidence that dinoflagellate genomes are extraordinarily impacted by HGT.

Keywords: Alexandrium tamarense Group IV; de novo transcriptome assembly; gene innovation; mitochondrial metabolism; phylogenetic profile; phylogenomics.

Fig. 1.—

Rarefaction curve showing the effect of adding raw sequence input (in billions of basepairs) on the Alexandrium tamarense Group IV de novo transcriptome assembly. Assembly length was measured in millions of basepairs. Number of sequences is illustrated both in terms of number of contigs in the full assembly and number of Oases loci.

Fig. 2.—

Ancestral gene content reconstruction of KOs. For both WP and DP analyses, bars and numbers to the right of the vertical axis represent the number of gene families gained at a branch relative to its parent. Bars and numbers to the left of the axis represent the number of gene families lost. The solid bar represents the net effect, either gain or loss of gene families, at each branch. LCA, last common ancestor; DALCA, dinoflagellate, apicomplexan LCA; SALCA, stramenopile, alveolate LCA.

Fig. 3.—

Phylogenomic bargraph showing the distribution of gene trees supporting diverse phylogenetic associations between dinoflagellates and other groups of organisms. Species tree is provided for reference, left. Bars represent putative categories based on the phylogenetic profile of the 17 species used in the KEGG ancestral gene content reconstruction (for list of species see fig. 2). The ubiquitous set (gray bars) represents genes found in all 17 species. The algal set (green bars) represents genes found in Alexandrium tamarense Group IV and the other five algal species. The dinoflagellate set (red bars) represents genes present in A. tamarense Group IV and absent from the other 16 genomes. These putative categories were compared with the phylogenomic results, which included sequences from many more organisms. DAC, dinoflagellate, apicomplexan clade.