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The mitochondrial gene order of Ascidiacea : extreme variability both within the class and compared to other deuterostomes
No full textA survey of mitochondrial evolution in Metazoa : large variability in little genomes
No full textThe animal mitochondrial genome (mtDNA) has been traditionally used as molecular marker for phylogenetic reconstructions but the study of the evolutionary history of this small genome can also help to unravel the hidden link between structural and functional genomic features. In this respect, the animal mtDNA can be regarded as a model in comparative genomics, whose use is also enhanced by the availability of complete sequences for about 2000 species. In spite of the biased taxon sampling, the analysis of the present mtDNA dataset is doubtless promising to reconstruct the evolutionary history of this entire genome in a wide phylogenetic range and to identify possible differences in its evolutionary trend among different lineages.
In order to carefully analyze the plethora of available mt sequences of Metazoa, we have developed a specialized mtDNA database, MitoZoa, collecting (nearly) complete mtDNA genomes whose annotations have been significantly corrected/improved using a semi-automatic reannotation pipeline. MitoZoa has been designed both to address comparative analyses of genomic features, such as gene order, non-coding regions and gene content, and to help comparisons at short evolutionary distances, such as in congeneric species. Here, we will briefly present the MitoZoa database and the preliminary results of our investigation on the mtDNA evolutionary dynamics in Metazoa: we have got insight into the variability of basic mitogenomic features, such as gene content, gene compactness, and base composition, and into the trend of gene order rearrangements in the main metazoan lineages. Especially in fast-evolving lineages, the same features have also been investigated in congeneric species, i.e. in closely-related species where saturation of evolutionary changes is unlikely to occur. Our data show that the mtDNA plasticity of Metazoa is higher that previously thought and that the mt evolutionary trend has changed several times, and sometimes dramatically, in the metazoan phylogenetic tree
A combined approach for successful reannotation of animal mitochondrial tRNAs based on pattern-matching and tRNA-predictor programs
No full textMotivation.
Transfer RNAs encoded by the mitochondrial genome (mtDNA) of Metazoa present strong deviations from the classical cloverleaf secondary structure, including the loss or size variation of either D- or T-domain. In addition, some taxa show “bizarre” tRNA structures: nematodes possess unconventional mt-tRNAs lacking either the T or D stem (1); spiders (Araneae, Chelicerata) and gall midges (Cecidomiiydae, Insecta) have many “truncated” tRNAs, i.e. tRNAs lacking a well-paired aminoacyl stem, which can also lost the T-arm (2,3); annelids belonging to family Questidae have a full set of truncated tRNAs (4).
These peculiarities hamper the annotation of mt-tRNAs in mtDNA sequences, since conventional tRNA detection programs perform poorly (as tRNAscan-SE) or lead to the detection of a significant number of false positives (as Arwen) (5,6). Finally, mt-tRNA annotations of are affected by numerous errors in gene name, boundaries and strand definition occurring during the sequence submission to primary databases (7). In the effort to construct a curated database of complete mtDNAs of Metazoa, we have developed a specific pipeline including both pattern-matching and tRNA-predictor programs, aimed at automatically check/rectify the annotation of both standard and “bizarre” mt-tRNAs.
Methods.
The developed mt-tRNA reannotation pipeline analyses the single tRNA sequences through two different programs: PatSearch, a pattern-matching program (8); and Arwen, a mt-tRNA secondary structure predictor (6). Two modules, made of several home-made Python scripts, specifically parse the results of PatSearch and Arwen using several empirically-settled criteria.
As for PatSearch, two main tRNAs patterns were specifically set for each mt-tRNA category. These patterns are able to detect the overall tRNA secondary structure based on the identification of only the aminoacyl (AA) and anticodon (AC) arms: the first pattern assumes perfectly annotated tRNAs with correct limits and a single 3'-discriminant base in the AA stem, while the second pattern searches for tRNAs having incorrect boundaries. In addition, patterns looking for a perfect AC arm in the correct tRNA position were also defined in order to look for “truncated” tRNAs, only in taxa where such unusual tRNA structures are expected to be present (Araneae, Cecidomiiydae and Questidae). All mt-tRNA patterns assume the presence of canonical anticodon sequences.
In this pipeline, Arwen was preferred to tRNAscan-SE because it has a detection rate close to 100% for mt-tRNAs, however, given the high false positive rate, Arwen results were taken into account only for mt-tRNAs not identified by the PatSearch patterns. Arwen itself has the advantage to find tRNAs with unusual anticodons and uncommon secondary structures, moreover the program was run applying specific options and extending the original tRNA boundaries from 5 to 45 bp at both gene sides, using an incremental step of 5 or 15 bp. The extension of the original tRNA boundaries forced the program to identify mt-tRNAs having erroneous gene limits.
Results.
A total dataset of 42,617 mt-tRNA sequences collected in the MitoZoa database v2.0 (9) was analyzed by our pipeline: 95.9% mt-tRNAs were identified/corrected by the PatSearch module; 3.8% were identified/corrected only by the Arwen module; 0.3% of the total tRNAs were not identified at the end of the whole pipeline and correspond mainly to erroneously annotated tRNAs. Thus, our pipeline represents a reliable tool for improving the annotation quality of metazoan mt-tRNAs both in complete and partial mtDNA sequences, since it was able to resolve (i.e. correct or validate) the annotation of >99% of the analyzed sequences, taking into account either taxon-specific and secondary-structure peculiarities of tRNA genes.
In order to compare the resolving power and accuracy of the two-core modules of our pipeline, the PatSearch-confirmed tRNAs (42,617 minus the 184 “truncated” tRNAs) were re-analyzed by the Arwen module. The results were straightforward: only 0.06% mt-tRNAs were predicted with different gene name/strand by the PatSearch compared to the Arwen module (these cases will be fully discussed in the poster), while 1.5% mt-tRNAs identified by PatSearch were not found by the Arwen module. This is mainly due to the low detection rate of Arwen for tRNA-Ser(AGY), tRNA-Cys and nematode mt-tRNAs, which together correspond to 44% of the total tRNAs not identified by Arwen. Among the 184 “truncated” tRNAs, all sequences were found by the PatSearch-settled patterns, while only 64 tRNAs (34.8%) were identified by the Arwen module. These results demonstrate that adequate patterns describing the tRNA secondary structure outperforms a good tRNA predictor such as Arwen in the present mt-tRNA reannotation pipeline, and could be useful for the identification of tRNA-like structure.
Supplementary information
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2.Beckenbach, A. and Joy, J. (2010) Genome Biology and Evolution, in press, 278-287.
3.Masta, S. and Boore, J. (2008) Mol Biol Evol, 25, 949-959.
4.Bleidorn, C., Hill, N., Erséus, C. and Tiedemann, R. (2009) Mol Phylogenet Evol., 52, 57-69.
5.Lowe, T.M. and Eddy, S.R. (1997) Nucleic Acids Res., 25, 955-964.
6.Laslett, D. and Canback, B. (2008) Bioinformatics., 24, 172-175.
7.Boore, J. (2006) OMICS, 10, 119-126.
8.Grillo G., Licciulli F., Liuni S., Sbisà E., Pesole G. (2003) Nucleic Acids Res. 31(13),3608-12.
9.Lupi, R., D'Onorio de Meo, P., Picardi, E., D'Antonio, M., Paoletti, D., Castrignanò, T., Pesole, G. and Gissi, C. (2010) Mitochondrion, 10, 192-199
Evolutionary mitogenomics of Chordata: the strange case of ascidians and vertebrates
No full textThe availability of almost one thousand complete mitochondrial genome (mtDNA) sequences of chordates provides an almost unique opportunity to analyse the evolution of this genome in the phylum Chordata, and to identify possible divergent evolutionary trends followed by the three chordate subphyla: Vertebrata, Cephalochordata and Tunicata.Here, we review some genome-level features of mtDNA, such as genetic code, gene content, genome architecture and gene strand asymmetry, mostly focusing on differences existing between tunicates and remaining chordates. Indeed, tunicate mtDNAs show a surprisingly high variability in several genome-level features, even though the current tunicate taxon sampling is absolutely insufficient and is focused mainly on the class Ascidiacea. On the contrary, a stabilization of the mtDNA structural and evolutionary features is observed in both cephalochordates and vertebrates, where genome-level features are almost invariant. Thus, different evolutionary dynamics, probably related to divergent functional constraints, have modelled the overall mtDNA structure and organization of the three chordate subphyla
One ring to divide them all : mitochondrial genomics unveils two cryptic species in Ciona intestinalis
No full text
Mitogenomics reveals a remarkably high intra-species substitution rate in the ascidian Botryllus schlosseri
No full textThe leitmotiv of mitochondrial genome (mtDNA) evolution in ascidians is the
hypervariability of many genomic features (such as gene order, nucleotide substitution
rate and tRNA gene content) even at short phylogenetic distances. As consequence, the
ascidian mtDNA has been proved to unambiguously discriminate between two cryptic
species of Ciona intestinalis. Here, we describe the mtDNA of a model species, the
colonial ascidian Botryllus schlosseri. Two specimens, one from California and one
from Italy, have been sequenced. We found that the mtDNA of B. schlosseri has a novel
gene order, completely different from other ascidians, and encodes for peculiar tRNAlike
structures. Surprisingly, the sequence divergence between the two specimens is up
to one order of magnitude higher (depending on the functional mt region) than the one
measured in other ascidian intra-species comparisons. However, this value is lower than
the one measured within genera, and between the two cryptic C. intestinalis species.
Thus, based on mtDNA, the Californian and Italian B. schlosseri specimens appear to
belong to a single species that is characterized by a remarkably high nucleotide
substitution rate
Mitochondrial phylogeny of Anura (Amphibia) : a case study of congruent phylogenetic reconstruction using amino acid and nucleotide characters
No full textWe explore whether phylogenetic analyses of the same sequence data set at the amino acid and nucleotide level are able to recover congruent topologies, as well as the advantages and limitations of both alternative approaches. As a case study, mitochondrial protein-coding genes were used to discern among competing hypotheses on the phylogenetic relationships of major anuran amphibian lineages. To properly address this phylogenetic question, the complete nucleotide sequences of the mitochondrial genomes of two archaeobatrachian species, Ascaphus truei and Pelobates cultripes, were determined anew. Bayesian and maximum likelihood phylogenetic inferences of the same sequence data set were performed based on both amino acid and nucleotide characters, with the latter analysed either as codons or as a reduced data set of first+second (P12) codon positions. In addition, likelihood-based ratio tests were performed to evaluate the support of alternative topologies. The different data sets arrived at congruent and highly supported topologies, suggesting a similar phylogenetic resolving power of the two character types provided that correctly selected sites and appropriate evolutionary models are used. The reconstructed anuran mitochondrial phylogeny supports the paraphyly of Archaeobatrachia, with Ascaphus as sister group to all the remaining anurans, and Pelobates as sister group of Neobatrachia. However, the employed tree reconstruction methods and likelihood-based ratio tests seemed to be negatively affected by the fast evolving sequences of neobatrachians, suggesting that the phylogeny of Anura here presented is not definitive, and needs further investigation using an extended taxon sampling
The fast evolutionary dynamics of ascidian mitochondrial genome: an exception to the general deuterostome evolutionary trend
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