Abstract

BackgroundMitochondria 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 FindingsThe 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/SignificanceOverall, 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.

Highlights

  • Reduction is a universal theme in the symbiotic events that gave rise to mitochondrial and plastid diversity

  • From the A+T-rich fraction of DNA of D. baltica and K. foliaceum, 299 and 635 pyrosequencing reads with an average length of 366 bp and 386 bp were respectively identified as endosymbiont mitochondrial sequences

  • A total of 169 and 123 Sanger reads were used in the assemblies, resulting in single contigs of 35,505 bp (D. baltica) and 39,686 bp (K. foliaceum) with an overall coverage of 5.466 and 7.736, respectively

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Summary

Introduction

Reduction is a universal theme in the symbiotic events that gave rise to mitochondrial and plastid diversity. The a–proteobacterial and cyanobacterial ancestors of mitochondria and plastids were drastically reduced to organelles that encode only a small fraction of their original genes [1,2,3,4]. In plastid evolution, this was followed by further rounds of primary and secondary endosymbiosis. 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

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