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. 2018 Jun 1;10(6):1504-1515.
doi: 10.1093/gbe/evy103.

Recurrent Loss, Horizontal Transfer, and the Obscure Origins of Mitochondrial Introns in Diatoms (Bacillariophyta)

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Free PMC article

Recurrent Loss, Horizontal Transfer, and the Obscure Origins of Mitochondrial Introns in Diatoms (Bacillariophyta)

Wilson X Guillory et al. Genome Biol Evol. .
Free PMC article

Abstract

We sequenced mitochondrial genomes from five diverse diatoms (Toxarium undulatum, Psammoneis japonica, Eunotia naegelii, Cylindrotheca closterium, and Nitzschia sp.), chosen to fill important phylogenetic gaps and help us characterize broadscale patterns of mitochondrial genome evolution in diatoms. Although gene content was strongly conserved, intron content varied widely across species. The vast majority of introns were of group II type and were located in the cox1 or rnl genes. Although recurrent intron loss appears to be the principal underlying cause of the sporadic distributions of mitochondrial introns across diatoms, phylogenetic analyses showed that intron distributions superficially consistent with a recurrent-loss model were sometimes more complicated, implicating horizontal transfer as a likely mechanism of intron acquisition as well. It was not clear, however, whether diatoms were the donors or recipients of horizontally transferred introns, highlighting a general challenge in resolving the evolutionary histories of many diatom mitochondrial introns. Although some of these histories may become clearer as more genomes are sampled, high rates of intron loss suggest that the origins of many diatom mitochondrial introns are likely to remain unclear.

Figures

<sc>Fig</sc>. 1.
Fig. 1.
—Unrooted phylogenetic trees for five intron groups (see supplementary table S2, Supplementary Material online) from the cox1 (A–D) and rnl genes (E), each of which contained at least five total sequences from our data set and GenBank’s nr database. Most of the 37 cox1 and rnl introns in our analysis have very few matches to sequenced genomes outside of diatoms. Additional details about these intron groups (e.g., cox1_g2_A) are available in supplementary table S2, Supplementary Material online, and trees with full taxon labels are shown in supplementary figure S1, Supplementary Material online. Diatoms are shown in black, and nondiatoms are shown in gray. Asterisks highlight nodes with bootstrap values >70%.
<sc>Fig</sc>. 2.
Fig. 2.
—Spatial and phylogenetic distributions of introns in the cox1 gene. Groups of putative homologs share similarly colored triangles, and unfilled triangles represent species-specific introns without homologs in other species in our analysis. Each unique insertion site is marked with a dashed vertical line. All introns are of type group II except for a single group I intron (marked with a “I”) in Kryptoperidinium. The phylogeny is a reference organismal tree compiled from previous studies (Theriot et al. 2015; Parks et al. 2018). Species marked with an asterisk (*) are the hosts for endosymbiotic diatoms. Major taxonomic groups referred to in the main text are identified (“Thal” = Thalassiosirales, “Bacillario.” = Bacillariophyceae).
<sc>Fig</sc>. 3.
Fig. 3.
—Maximum likelihood phylogeny of the cox1_g2_B intron group. Diatoms are shown on purple branches, and nondiatom stramenopiles are shown on gray branches. The alignment included introns with two different insertion sites in the cox1 gene, shown by the positions of the purple triangles on a depiction of the cox1 coding sequences (A), similar to what is shown in figure 2. Asterisks represent 100% bootstrap support. Panel (B) shows pairwise sequence similarities between the raphidophyte, Chattonella, and each diatom in the cox1_g2_A and cox1_g2_B intron groups. For species in the cox1_g2_A group, introns uniformly show lower sequence similarity than exons. For species in the cox1_g2_B group, pairwise sequence similarities in exons were similar to what was found in cox1_g2_A, but there was a much broader range of intron similarities, with two species, Cylindrotheca and C. nana, possessing introns that were > 94% similar to the homologous copy in Chattonella; a small amount of random vertical scatter was introduced to better display the values of overlapping data points (B).
<sc>Fig</sc>. 4.
Fig. 4.
—Spatial and phylogenetic distributions of introns in the rnl gene. Groups of putative homologs share similarly shaded triangles, and unfilled triangles represent species-specific introns without homologs in other species in our analysis. Each unique insertion site is marked with a dashed vertical line. All introns are of type group II except for a single group I intron (marked with a “I”) in Kryptoperidinium. The phylogeny is a reference organismal tree compiled from previous studies (Theriot et al. 2015; Parks et al. 2018). Species marked with an asterisk (*) are the hosts for endosymbiotic diatoms.

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