Towards a comprehensive picture of alloacceptor tRNA remolding in metazoan mitochondrial genomes

Sahyoun, Abdullah H.; Hölzer, Martin; Jühling, Frank; Siederdissen, Christian Höner zu; Al-Arab, Marwa; Tout, Kifah; Marz, Manja; Middendorf, Martin; Stadler, Peter F.; Bernt, Matthias

doi:10.1093/nar/gkv746

Cited by 24 publications

(15 citation statements)

References 68 publications

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“…As a result, the mitogenome now possesses what appear to be two functional tRNA-Trp genes. Remolding of tRNAs is a well-documented process that involves a duplication of a tRNA gene, a mutation that changes the anticodon and the loss of the ancestral tRNA gene [ 54 ], but in this case there is no indication that tRNA-Ser2 was duplicated in the first place. Suspecting a sequencing artefact, we have checked the electropherogram, but there was no indication of poor sequencing quality either.…”

Section: Resultsmentioning

confidence: 99%

The complete mitochondrial genome of parasitic nematode Camallanus cotti: extreme discontinuity in the rate of mitogenomic architecture evolution within the Chromadorea class

et al. 2017

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BackgroundComplete mitochondrial genomes are much better suited for the taxonomic identification and phylogenetic studies of nematodes than morphology or traditionally-used molecular markers, but they remain unavailable for the entire Camallanidae family (Chromadorea). As the only published mitogenome in the Camallanina suborder (Dracunculoidea superfamily) exhibited a unique gene order, the other objective of this research was to study the evolution of mitochondrial architecture in the Spirurida order. Thus, we sequenced the complete mitogenome of the Camallanus cotti fish parasite and conducted structural and phylogenomic comparative analyses with all available Spirurida mitogenomes.ResultsThe mitogenome is exceptionally large (17,901 bp) among the Chromadorea and, with 46 (pseudo-) genes, exhibits a unique architecture among nematodes. Six protein-coding genes (PCGs) and six tRNAs are duplicated. An additional (seventh) tRNA (Trp) was probably duplicated by the remolding of tRNA-Ser2 (missing). Two pairs of these duplicated PCGs might be functional; three were incomplete and one contained stop codons. Apart from Ala and Asp, all other duplicated tRNAs are conserved and probably functional. Only 19 unique tRNAs were found. Phylogenomic analysis included Gnathostomatidae (Spirurina) in the Camallanina suborder.ConclusionsWithin the Nematoda, comparable PCG duplications were observed only in the enoplean Mermithidae family, but those result from mitochondrial recombination, whereas characteristics of the studied mitogenome suggest that likely rearrangement mechanisms are either a series of duplications, transpositions and random loss events, or duplication, fragmentation and subsequent reassembly of the mitogenome. We put forward a hypothesis that the evolution of mitogenomic architecture is extremely discontinuous, and that once a long period of stasis in gene order and content has been punctuated by a rearrangement event, such a destabilised mitogenome is much more likely to undergo subsequent rearrangement events, resulting in an exponentially accelerated evolutionary rate of mitogenomic rearrangements. Implications of this model are particularly important for the application of gene order similarity as an additive source of phylogenetic information. Chromadorean nematodes, and particularly Camallanina clade (with C. cotti as an example of extremely accelerated rate of rearrangements), might be a good model to further study this discontinuity in the dynamics of mitogenomic evolution.Electronic supplementary materialThe online version of this article (doi: 10.1186/s12864-017-4237-x) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

The complete mitochondrial genome of parasitic nematode Camallanus cotti: extreme discontinuity in the rate of mitogenomic architecture evolution within the Chromadorea class

et al. 2017

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“…Evidence of tRNA remolding was found in mitochondrial genomes of different groups, including Porifera [88–91], Mollusca [92, 93], Echinodermata [87], Arthropoda [43, 91], Chordata [94, 95]. It was recently shown that the remolding event of Trp (UCA) to Gly (UCC) took place in the ancestor of amphipods [91].…”

Section: Resultsmentioning

confidence: 99%

“…It was recently shown that the remolding event of Trp (UCA) to Gly (UCC) took place in the ancestor of amphipods [91]. Additional tRNA copies found in the mitogenomes of Baikalian amphipods illustrate different stages of the rearrangement process.…”

Section: Resultsmentioning

confidence: 99%

Evolution of mitochondrial genomes in Baikalian amphipods

et al. 2016

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BackgroundAmphipods (Crustacea) of Lake Baikal are a very numerous and diverse group of invertebrates generally believed to have originated by adaptive radiation. The evolutionary history and phylogenetic relationships in Baikalian amphipods still remain poorly understood. Sequencing of mitochondrial genomes is a relatively feasible way for obtaining a set of gene sequences suitable for robust phylogenetic inferences. The architecture of mitochondrial genomes also may provide additional information on the mechanisms of evolution of amphipods in Lake Baikal.ResultsThree complete and four nearly complete mitochondrial genomes of Baikalian amphipods were obtained by high-throughput sequencing using the Illumina platform. A phylogenetic inference based on the nucleotide sequences of all mitochondrial protein coding genes revealed the Baikalian species to be a monophyletic group relative to the nearest non-Baikalian species with a completely sequenced mitochondrial genome - Gammarus duebeni. The phylogeny of Baikalian amphipods also suggests that the shallow-water species Eulimnogammarus has likely evolved from a deep-water ancestor, however many other species have to be added to the analysis to test this hypothesis.The gene order in all mitochondrial genomes of studied Baikalian amphipods differs from the pancrustacean ground pattern. Mitochondrial genomes of four species possess 23 tRNA genes, and in three genomes the extra tRNA gene copies have likely undergone remolding. Widely varying lengths of putative control regions and other intergenic spacers are typical for the mitochondrial genomes of Baikalian amphipods.ConclusionsThe mitochondrial genomes of Baikalian amphipods display varying organization suggesting an intense rearrangement process during their evolution. Comparison of complete mitochondrial genomes is a potent approach for studying the amphipod evolution in Lake Baikal.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3357-z) contains supplementary material, which is available to authorized users.

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“…This process has been extensively documented in both bilaterian and nonbilaterian animal mtDNA (Lavrov and Lang 2005; Wang and Lavrov 2011; Sahyoun et al 2015). …”

Section: Loss and Gain Of Mitochondrial Trna Genesmentioning

confidence: 97%

Animal Mitochondrial DNA as We Do Not Know It: mt-Genome Organization and Evolution in Nonbilaterian Lineages

2016

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Animal mitochondrial DNA (mtDNA) is commonly described as a small, circular molecule that is conserved in size, gene content, and organization. Data collected in the last decade have challenged this view by revealing considerable diversity in animal mitochondrial genome organization. Much of this diversity has been found in nonbilaterian animals (phyla Cnidaria, Ctenophora, Placozoa, and Porifera), which, from a phylogenetic perspective, form the main branches of the animal tree along with Bilateria. Within these groups, mt-genomes are characterized by varying numbers of both linear and circular chromosomes, extra genes (e.g. atp9, polB, tatC), large variation in the number of encoded mitochondrial transfer RNAs (tRNAs) (0–25), at least seven different genetic codes, presence/absence of introns, tRNA and mRNA editing, fragmented ribosomal RNA genes, translational frameshifting, highly variable substitution rates, and a large range of genome sizes. This newly discovered diversity allows a better understanding of the evolutionary plasticity and conservation of animal mtDNA and provides insights into the molecular and evolutionary mechanisms shaping mitochondrial genomes.

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Towards a comprehensive picture of alloacceptor tRNA remolding in metazoan mitochondrial genomes

Cited by 24 publications

References 68 publications

The complete mitochondrial genome of parasitic nematode Camallanus cotti: extreme discontinuity in the rate of mitogenomic architecture evolution within the Chromadorea class

The complete mitochondrial genome of parasitic nematode Camallanus cotti: extreme discontinuity in the rate of mitogenomic architecture evolution within the Chromadorea class

Evolution of mitochondrial genomes in Baikalian amphipods

Animal Mitochondrial DNA as We Do Not Know It: mt-Genome Organization and Evolution in Nonbilaterian Lineages

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