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, 7 (8), e43763

Tertiary Endosymbiosis in Two Dinotoms Has Generated Little Change in the Mitochondrial Genomes of Their Dinoflagellate Hosts and Diatom Endosymbionts

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Tertiary Endosymbiosis in Two Dinotoms Has Generated Little Change in the Mitochondrial Genomes of Their Dinoflagellate Hosts and Diatom Endosymbionts

Behzad Imanian et al. PLoS One.

Abstract

Background: Mitochondria or mitochondrion-derived organelles are found in all eukaryotes with the exception of secondary or tertiary plastid endosymbionts. In these highly reduced systems, the mitochondrion has been lost in all cases except the diatom endosymbionts found in a small group of dinoflagellates, called 'dinotoms', the only cells with two evolutionarily distinct mitochondria. To investigate the persistence of this redundancy and its consequences on the content and structure of the endosymbiont and host mitochondrial genomes, we report the sequences of these genomes from two dinotoms.

Methodology/principal findings: The endosymbiont mitochondrial genomes of Durinskia baltica and Kryptoperidinium foliaceum exhibit nearly identical gene content with other diatoms, and highly conserved gene order (nearly identical to that of the raphid pennate diatom Fragilariopsis cylindrus). These two genomes are differentiated from other diatoms' by the fission of nad11 and by an insertion within nad2, in-frame and unspliced from the mRNA. Durinskia baltica is further distinguished from K. foliaceum by two gene fusions and its lack of introns. The host mitochondrial genome in D. baltica encodes cox1 and cob plus several fragments of LSU rRNA gene in a hugely expanded genome that includes numerous pseudogenes, and a trans-spliced cox3 gene, like in other dinoflagellates. Over 100 distinct contigs were identified through 454 sequencing, but intact full-length genes for cox1, cob and the 5' exon of cox3 were present as a single contig each, suggesting most of the genome is pseudogenes. The host mitochondrial genome of K. foliaceum was difficult to identify, but fragments of all the three protein-coding genes, corresponding transcripts, and transcripts of several LSU rRNA fragments were all recovered.

Conclusions/significance: Overall, the endosymbiont and host mitochondrial genomes in the two dinotoms have changed surprisingly little from those of free-living diatoms and dinoflagellates, irrespective of their long coexistence side by side in dinotoms.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. The mitochondrial genome maps of the endosymbionts in Durinskia baltica and Kryptoperidinium foliaceum.
Functionally related genes are colour-coded and transcriptional direction is clockwise (boxes outside the ring) or counterclockwise (inside). Genes for tRNAs are indicated by their single letter code. The dashed lines represent the gap in the genomes. The blue arrows specify the locations of the introns in the map for K. foliaceum, and the red arrows point at the locations of gene fusions in the map of D. baltica. The arcs show the conserved gene blocks in the two dinotoms and P. tricornutum (green and orange arcs) and T. pseudonana (the green arcs). The two genomes are not represented in scale with respect to one another.
Figure 2
Figure 2. Predicted secondary structure of the three Kryptoperidinium foliaceum endosymbiont mitochondrial introns modeled according to the conventions described in Burke et al.
and Michel et al. . (A) Group I introns. Left, the first cox1 intron; Right, the rnl intron. The K. foliaceum cox1 group I intron (left) had been previously mistakenly referred to as a group II intron . (B) Group II intron. The second cox1 intron. Panels A and B: canonical Watson-Crick base pairings are denoted by dashes whereas guanine-uracyl pairings are marked by dots. Numbers inside variable loops indicate the sizes of these loops. Exon sequences are shown in lowercase letters. Panel A: splice sites between exon and intron residues are denoted by arrows; Panel B: the major structural domains are indicated by roman numerals and capital letters A to D, whereas tertiary interactions are represented by dashed lines, curved arrows, and/or Greek letters. Nucleotides potentially involved in the δ-δ′ interaction are boxed. Intron-binding and exon-binding sites are indicated by IBS and EBS, respectively. The putative site of lariat formation is denoted by an asterisk.
Figure 3
Figure 3. Genes and their pseudogenes in the mitochondrial genome of Durinskia baltica.
(A) The full-length genes and their derived pseudogenes. The full-length protein-coding genes and the LSU rRNA gene fragments are represented by colored blocks, while the pseudogenes are shown by colored blocks with a broken tip. The lines represent non-coding sequences. The genes and their matching sequences within the pseudogenes are color-coded: cox1 in red; cob in blue; cox3 in green; LSU rRNA fragments in yellow. The sequences are drawn in scale. The numbers at the bottom of the contigs show their sizes in nucleotides, while the numbers on the top within parentheses specify the number of the first and last amino acids on the full-length gene corresponding to the conserved sequences of the pseudogenes. (B) The Alignment of the conserved regions of many pseudogenes with their corresponding full-length gene.

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Grant support

This work was supported by a grant [227301] from the Natural Sciences and Engineering Research Council of Canada (NSERC). BI is supported by a doctoral scholarship from NSERC and J-FP by a Louis-Berlinguet Postdoctoral Fellowship from the Fonds Québécois de la Recherche sur la Nature et les Technologies/Génome Québec. PJK is a Fellow of the Canadian Institute for Advanced Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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