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

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.

Endosymbiotic Gene Transfer in Tertiary Plastid-Containing Dinoflagellates

“…On the other hand, the low level of EGT observed in dinotoms puts their endosymbiont on the periphery of the organelle definition, since it is fully integrated within the cell in many ways but not deeply integrated on a genetic level. Thus, in addition to challenging our view of how we define endosymbionts and organelles, this also reinforces the idea that dinotoms may represent an unusual intermediate in the continuum of symbiotic interactions observed in nature (51,105,106). …”

Integration of plastids with their hosts: Lessons learned from dinoflagellates

“…This genome is permanently condensed and uses an unusual DNA packaging protein that is evolutionarily distinct from histones (15). The dinoflagellate mitochondrial genome is likewise highly abnormal, containing only three protein-coding genes (cob, coxI, and coxIII), which are present in multiple, fragmented copies (16,17).…”

“…The genomes of the endosymbiont mitochondria of both dinotoms have also been sequenced (17). The dinotom plastid and endosymbiont mitochondrial genomes are similar to those of free-living diatoms, with almost no examples of gene loss (Fig.…”

“…Not only is the endosymbiont largely unreduced in terms of genome content (17,64), there is no significant evidence for the presence of genes in the host nucleus-of any phylogenetic derivation-that are likely to support the plastid (65,66,74). It seems instead that the endosymbiont nucleus plays a more significant role in supporting the plastid (65,66).…”

Peculiarities within peculiarities – dinoflagellates and their mitochondrial genomes

“…of reef-building corals (G omez 2012). They are distinguished by a number of peculiarities, among them the unique mitogenome and, in some cases, even two functional mitochondrial sets in one cell: one of their own and the second present in an engulfed endosymbiotic diatom (Imanian et al 2012;Gagat et al 2014). Together with their sister parasitic lineage Apicomplexa and some other relatives, dinoflagellates constitute the Myzozoa assemblage that unites with free-living ciliates in the superphylum Alveolata (Figure 1; Burki 2014).…”