Tertiary Endosymbiosis in Two Dinotoms Has Generated Little Change in the Mitochondrial Genomes of Their Dinoflagellate Hosts and Diatom Endosymbionts (original) (raw)
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Peculiarities within peculiarities – dinoflagellates and their mitochondrial genomes
Mitochondrial DNA Part B, 2017
After the establishment of an endosymbiotic relationship between a proto-mitochondrion and its probable archaeal host, mitochondrial genomes underwent a spectacular reductive evolution. An interesting pathway was chosen by mitogenomes of unicellular protists called dinoflagellates, which experienced an additional wave of reduction followed by amplification and rearrangement leading to their secondary complexity. The former resulted in a mitogenome consisting of only three protein-coding genes, the latter in their multiple copies being scattered across numerous chromosomes and the evolution of complex processes for their expression. These stunning features raise a question about the future of the dinoflagellate mitochondrial genome.
BMC Evolutionary Biology, 2007
The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum are distinguished by the presence of a tertiary plastid derived from a diatom endosymbiont. The diatom is fully integrated with the host cell cycle and is so altered in structure as to be difficult to recognize it as a diatom, and yet it retains a number of features normally lost in tertiary and secondary endosymbionts, most notably mitochondria. The dinoflagellate host is also reported to retain mitochondrion-like structures, making these cells unique in retaining two evolutionarily distinct mitochondria. This redundancy raises the question of whether the organelles share any functions in common or have distributed functions between them.
The mitochondrial genome and the expression of the genes within it have evolved to be highly unusual in several lineages. Within alveolates, apicomplexans and dinoflagellates share the most reduced mitochondrial gene content on record, but differ from one another in organisation and function. To clarify how these characteristics originated, we examined mitochondrial genome form and expression in a key lineage that arose close to the divergence of apicomplexans and dinoflagellates, Oxyrrhis marina.We show that Oxyrrhis is a basal member of the dinoflagellate lineage whose mitochondrial genome has some unique characteristics while sharing others with apicomplexans or dinoflagellates. Specifically, Oxyrrhis has the smallest gene complement known, with several rRNA fragments and only two protein coding genes, cox1 and a cob-cox3 fusion. The genome appears to be highly fragmented, like that of dinoflagellates, but genes are frequently arranged as tandem copies, reminiscent of the repeating nature of the Plasmodium genome. In dinoflagellates and Oxyrrhis, genes are found in many arrangements, but the Oxyrrhis genome appears to be more structured, since neighbouring genes or gene fragments are invariably the same: cox1 and the cob-cox3 fusion were never found on the same genomic fragment. Analysing hundreds of cDNAs for both genes and circularized mRNAs from cob-cox3 showed that neither uses canonical start or stop codons, although a UAA terminator is created in the cob-cox3 fusion mRNA by post-transcriptional oligoadenylation. mRNAs from both genes also use a novel 5' oligo(U) cap. Extensive RNA editing is characteristic of dinoflagellates, but we find no editing in Oxyrrhis. Overall, the combination of characteristics found in the Oxyrrhis genome allows us to plot the sequence of many events that led to the extreme organisation of apicomplexan and dinoflalgellate mitochondrial genomes.
Applied and Environmental Microbiology, 2008
Dinophysis acuminata cells were isolated from Narragansett Bay water samples in June 2005 using flow cytometry. Dinoflagellate-specific PCR primers were used to isolate small-subunit rRNA (18S rRNA), mitochondrial cytochrome b (cob), and cytochrome c oxidase I (cox1) genes and the encoded cDNAs. Maximumlikelihood analysis of a concatenated data set of ribosomal DNA and cDNA sequences of cob and cox1 showed that D. acuminata was sister to Gonyaulacoids, but without strong bootstrap support. The approximately unbiased test could not reject alternative positions of D. acuminata. To gain better resolution, mRNA editing of cob and cox1 was inferred for D. acuminata and 13 other dinoflagellate species. The location and type of editing as well as the distribution pattern in D. acuminata were generally similar to those in other dinoflagellates except for two edited sites that are unique to this species. Bayesian analyses of a matrix that recorded the location and type of editing, and of a matrix that included the protein sequences of COB and COX1 with the editing data yielded tree topologies similar to the three-gene tree but again failed to resolve the phylogenetic position of D. acuminata. However, the density of edited sites in the D. acuminata mitochondrial genes, consistent with phylogenetic trees, indicated that Dinophysis is a derived dinoflagellate lineage, diverging after other lineages such as Oxyrrhis, Amphidinium, and Symbiodinium. We demonstrate that dinoflagellate-specific PCR coupled with flow cytometry can be a useful tool to analyze genes and their transcripts from a natural dinoflagellate population.
Current Genetics, 2010
The first two mitochondrial genomes of marine diatoms were previously reported for the centric Thalassiosira pseudonana and the raphid pennate Phaeodactylum tricornutum. As part of a genomic project, we sequenced the complete mitochondrial genome of the freshwater araphid pennate diatom Synedra acus. This 46,657 bp mtDNA encodes 2 rRNAs, 24 tRNAs, and 33 proteins. The mtDNA of S. acus contains three group II introns, two inserted into the cox1 gene and containing ORFs, and one inserted into the rnl gene and lacking an ORF. The compact gene organization contrasts with the presence of a 4.9-kb-long intergenic region, which contains repeat sequences. Comparison of the three sequenced mtDNAs showed that these three genomes carry similar gene pools, but the positions of some genes are rearranged. Phylogenetic analysis performed with a fragment of the cox1 gene of diatoms and other heterokonts produced a tree that is similar to that derived from 18S RNA genes. The introns of mtDNA in the diatoms seem to be polyphyletic. This study demonstrates that pyrosequencing is an efficient method for complete sequencing of mitochondrial genomes from diatoms, and may soon give valuable information about the molecular phylogeny of this outstanding group of unicellular organisms.
Genome Biology and Evolution, 2012
The sister phyla dinoflagellates and apicomplexans inherited a drastically reduced mitochondrial genome (mitochondrial DNA, mtDNA) containing only three protein-coding (cob, cox1, and cox3) genes and two ribosomal RNA (rRNA) genes. In apicomplexans, single copies of these genes are encoded on the smallest known mtDNA chromosome (6 kb). In dinoflagellates, however, the genome has undergone further substantial modifications, including massive genome amplification and recombination resulting in multiple copies of each gene and gene fragments linked in numerous combinations. Furthermore, protein-encoding genes have lost standard stop codons, trans-splicing of messenger RNAs (mRNAs) is required to generate complete cox3 transcripts, and extensive RNA editing recodes most genes. From taxa investigated to date, it is unclear when many of these unusual dinoflagellate mtDNA characters evolved. To address this question, we investigated the mitochondrial genome and transcriptome character states of the deep branching dinoflagellate Hematodinium sp. Genomic data show that like later-branching dinoflagellates Hematodinium sp. also contains an inflated, heavily recombined genome of multicopy genes and gene fragments. Although stop codons are also lacking for cox1 and cob, cox3 still encodes a conventional stop codon. Extensive editing of mRNAs also occurs in Hematodinium sp. The mtDNA of basal dinoflagellate Hematodinium sp. indicates that much of the mtDNA modification in dinoflagellates occurred early in this lineage, including genome amplification and recombination, and decreased use of standard stop codons. Trans-splicing, on the other hand, occurred after Hematodinium sp. diverged. Only RNA editing presents a nonlinear pattern of evolution in dinoflagellates as this process occurs in Hematodinium sp. but is absent in some later-branching taxa indicating that this process was either lost in some lineages or developed more than once during the evolution of the highly unusual dinoflagellate mtDNA.
The Complete Plastid Genomes of the Two ‘Dinotoms’ Durinskia baltica and Kryptoperidinium foliaceum
PLoS ONE, 2010
Background: In one small group of dinoflagellates, photosynthesis is carried out by a tertiary endosymbiont derived from a diatom, giving rise to a complex cell that we collectively refer to as a 'dinotom'. The endosymbiont is separated from its host by a single membrane and retains plastids, mitochondria, a large nucleus, and many other eukaryotic organelles and structures, a level of complexity suggesting an early stage of integration. Although the evolution of these endosymbionts has attracted considerable interest, the plastid genome has not been examined in detail, and indeed no tertiary plastid genome has yet been sequenced.
Journal of Molecular Evolution, 1997
The chloroplasts of euglenophytes and dinoflagellates have been suggested to be the vestiges of endosymbiotic algae acquired during the process of evolution. However, the evolutionary positions of these organisms are still inconclusive, and they have been tentatively classified as both algae and protozoa. A representative gene of the mitochondrial genome, cytochrome oxidase subunit I (coxI), was chosen and sequenced to clarify the phylogenetic positions of four dinoflagellates, two euglenophytes and one apicomplexan protist. This is the first report of mitochondrial DNA sequences for dinoflagellates and euglenophytes. Our COXI tree shows clearly that dinoflagellates are closely linked to apicomplexan parasites but not with algae. Euglenophytes and algae appear to be only remotely related, with euglenophytes sharing a possible evolutionary link with kinetoplastids. The COXI tree is in general agreement with the tree based on the nuclear encoded small subunit of ribosomal RNA (SSU rRNA) genes, but conflicts with that based on plastid genes. These results support the interpretation that chloroplasts present in euglenophytes and dinoflagellates were captured from algae through endosymbioses, while their mitochondria were inherited from the host cell. We suggest that dinoflagellates and euglenophytes were originally heterotrophic protists and that their chloroplasts are remnants of endosymbiotic algae.
INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, 2000
The marine dinoflagellates Peridinium balticum and Peridinium foliaceum are known for bearing diatom endosymbionts instead of peridinin-containing plastids. While evidence clearly indicates that their endosymbionts are closely related, the relationship between the host dinoflagellate cells is not settled. To examine the relationship of the two dinoflagellates, the DNA sequences of nuclear small-subunit rRNA genes (SSU rDNA) from Peridinium balticum, Peridinium foliaceum and one other peridinin-containing species, Peridinium bipes, were amplified, cloned and sequenced. While phylogenetic analyses under simple models of nucleotide substitution weakly support the monophyly of Peridinium balticum and Peridinium foliaceum, analyses under more sophisticated models significantly increased the statistical support for this relationship. Combining these results with the similarity between the two endosymbionts, it is concluded that (i) the two hosts have the closest sister relationship among dinoflagellates tested, (ii) the hypothesis that the diatom endosymbiosis occurred prior to the separation of the host cells is most likely to explain their evolutionary histories, and (iii) phylogenetic inferences under complex nucleotide evolution models seem to be able to compensate significant rate variation in the two SSU rDNA.
Widespread and Extensive Editing of Mitochondrial mRNAS in Dinoflagellates
Journal of Molecular Biology, 2002
We report evidence of extensive substitutional editing of mitochondrial mRNAs in the dinoflagellate species Pfiesteria piscicida, Prorocentrum minimum and Crypthecodinium cohnii, based on a comparison of genomic and corresponding cDNA sequences determined for two mitochondrial DNA-encoded genes, cox1 (cytochrome oxidase subunit 1) and cob (apocytochrome b ). In the cox1 mRNA, we identify 72 substitutions at 40 sites in 39 codons, whereas in cob mRNA, we infer 86 editing events at 51 sites in 48 codons. Editing, which takes place in distinct clusters, changes , 2% of the total sequence, occurs predominantly at first and second positions of codons, and involves mostly (but not exclusively) A ! G (47%), U ! C (23%) and C ! U (17%) substitutions. In all but four of the 158 cases, editing changes the identity of the specified amino acid. At 21 (cox1 ) and 26 (cob ) sites, the same nucleotide change is observed at the same position in at least two of the species investigated. At about onethird of the sites, editing results in an amino acid change that increases similarity between the dinoflagellate Cox1 and Cob sequences and their homologs in other organisms; presumably editing at these sites is of particular functional significance. Overall, about half of the editing events either maintain or increase similarity between the dinoflagellate protein sequences and their non-dinoflagellate homologs, while a further onethird of the alterations are "dinoflagellate-specific" (i.e. they involve a change to an amino acid residue selectively conserved in at least two of the dinoflagellate species at a given position). The nature, pattern and phylogenetic distribution of the inferred edits implies either that more than one type of previously described editing process operates on a given transcript in dinoflagellate mitochondria, or that a mechanistically unique type of mitochondrial mRNA editing has evolved within the dinoflagellate lineage.