The partial mitochondrial genome of the Cephalothrix rufifrons (Nemertea, Palaeonemertea): characterization and implications for the phylogenetic position of Nemertea

A continuous 10.1kb fragment of the Cephalothrix rufifrons (Nemertea, Palaeonemertea) mitochondrial genome was sequenced and characterized to further assess organization of protostome mitochondrial genomes and evaluate the phylogenetic potential of gene arrangement and amino acid characters. The genome is A-T rich (72%), and this biased base composition is partly reflected in codon usage. Inferred tRNA secondary structures are typical of those reported for other metazoan mitochondrial DNAs. The arrangement of the 26 genes contained in the fragment exhibits marked similarity to those of many protostome taxa, most notably molluscs with highly conserved arrangements and a phoronid. Separate and simultaneous phylogenetic analyses of inferred amino acid sequences and gene adjacencies place the nemertean within the protostomes among coelomate lophotrochozoan taxa, but do not find a well-supported sister taxon link.     

Big trees from little genomes: mitochondrial gene order as a phylogenetic tool

Gene arrangement comparisons are a powerful tool for phylogenetic studies, especially those focused on ancient relationships. Recent reports using metazoan mitochondrial genomes address evolutionary relationships as well as rates and mechanisms of rearrangement. Mitochondrial systems serve as a model for larger-scale comparisons of whole organismal genomes and a stimulus for developing methods for reconstructing the patterns of rearrangement.     

Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species

The mitochondrial genome (mtDNA) of Metazoa is a good model system for evolutionary genomic studies and the availability of more than 1000 sequences provides an almost unique opportunity to decode the mechanisms of genome evolution over a large phylogenetic range. In this paper, we review several structural features of the metazoan mtDNA, such as gene content, genome size, genome architecture and the new parameter of gene strand asymmetry in a phylogenetic framework. The data reviewed here show that: (1) the plasticity of Metazoa mtDNA is higher than previously thought and mainly due to variation in number and location of tRNA genes; (2) an exceptional trend towards stabilization of genomic features occurred in deuterostomes and was exacerbated in vertebrates, where gene content, genome architecture and gene strand asymmetry are almost invariant. Only tunicates exhibit a very high degree of genome variability comparable to that found outside deuterostomes. In order to analyse the genomic evolutionary process at short evolutionary distances, we have also compared mtDNAs of species belonging to the same genus: the variability observed in congeneric species significantly recapitulates the evolutionary dynamics observed at higher taxonomic ranks, especially for taxa showing high levels of genome plasticity and/or fast nucleotide substitution rates. Thus, the analysis of congeneric species promises to be a valuable approach for the assessment of the mtDNA evolutionary trend in poorly or not yet sampled metazoan groups.     

Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements

Phylogenetic relationships among the metazoan phyla are the subject of an ongoing controversy. Analysis of mitochondrial gene arrangements is a powerful tool to investigate these relationships; however, its previous application outside of individual animal phyla has been hampered by the lack of informative out-group data. To address this shortcoming, we determined complete mitochondrial DNA sequences for the demosponges Geodia neptuni and Tethya actinia, two representatives of the most basal animal phylum, the Porifera. With sponges as an outgroup, we investigated phylogenetic relationships of nine bilaterian phyla using both breakpoint analysis of global mitochondrial gene arrangements and maximum parsimony analysis of mitochondrial gene adjacencies. Our results provide strong support for a group that includes protostome (but not deuterostome) coelomate, pseudocoelomate, and acoelomate animals, thus clearly rejecting the Coelomata hypothesis. Two other groups of bilaterian animals, Lophotrochozoa and Ambulacraria, are also supported by our analyses. However, due to the remarkable stability of mitochondrial gene arrangements in Deuterostomia and the Ecdysozoa, conclusions on their evolutionary history cannot be drawn.     

Analysis of the complete mitochondrial DNA sequence of the brachiopod terebratulina retusa places Brachiopoda within the protostomes

Brachiopod phylogeny is still a controversial subject. Analyses using nuclear 18SrRNA and mitochondrial 12SrDNA sequences place them within the protostomes but some recent interpretations of morphological data support a relationship with deuterostomes. In order to investigate brachiopod affinities within the metazoa further, we compared the gene arrangement on the brachiopod mitochondrial genome with several metazoan taxa. The complete (15 451 bp) mitochondrial DNA (mtDNA) sequence of the articulate brachiopod Terebratulina retusa was determined from two overlapping long polymerase chain reaction products. All the genes are encoded on the same strand and gene order comparisons showed that.only one major rearrangement is required to interconvert the T. retusa and Katharina tunicata (Mollusca: Polvplacophora) mitochondrial genomes. The partial mtDNA sequence of the prosobranch mollusc Littorina saxatilis shows complete congruence with the T. rehtusa gene arrangement with regard to the ribosomal and protein coding genes. This high similarity in gene arrangement is the first to be reported within the protostomes. Sequence analyses of mitochondrial protein coding genes also support a close relationship of the brachiopod with molluscs and annelids, thus supporting the clade Lophotrochozoa. Though being highly informative, sequence analyses of the mitochondrial protein coding genes failed to resolve the branching order within the lophotrochozoa.     

Complete mitochondrial genome of Tubulipora flabellaris (Bryozoa: Stenolaemata): the first representative from the class Stenolaemata with unique gene order

Mitochondrial genomes play a significant role in the reconstruction of phylogenetic relationships within metazoans. There are still many controversies concerning the phylogenetic position of the phylum Bryozoa. In this research, we have finished the complete mitochondrial genome of one bryozoan (Tubulipora flabellaris), which is the first representative from the class Stenolaemata. The complete mitochondrial genome of T. flabellaris is 13,763 bp in length and contains 36 genes, which lacks the atp8 gene in contrast to the typical metazoan mitochondrial genomes. Gene arrangement comparisons indicate that the mitochondrial genome of T. flabellaris has unique gene order when compared with other metazoans. The four known bryozoans complete mitochondrial genomes also have very different gene arrangements, indicates that bryozoan mitochondrial genomes have experienced drastic rearrangements. To investigate the phylogenetic relationship of Bryozoa, phylogenetic analyses based on amino acid sequences of 11 protein coding genes (excluding atp6 and atp8) from 26 metazoan complete mitochondrial genomes were made utilizing Maximum Likelihood (ML) and Bayesian methods, respectively. The results indicate the monopoly of Lophotrochozoa and a close relationship between Chaetognatha and Bryozoa. However, more evidences are needed to clarify the relationship between two groups. Lophophorate appeared to be polyphyletic according to our analyses. Meanwhile, neither analysis supports close relationship between Branchiopod and Phoronida. Four bryozoans form a clade and the relationship among them is T. flabellaris + (F. hispida + (B. neritina + W. subtorquata)), which is in coincidence with traditional classification system.     

The complete mitochondrial genome sequence of Whitmania pigra (Annelida, Hirudinea): the first representative from the class Hirudinea

The mitochondrial genome is a significant tool for investigating the evolutionary history of metazoan animals. The currently available mitochondrial genome data in GenBank is limited to understand the detail evolutionary relationship among the metazoan animals, especially in the phylum Annelida. Here we present the mitochondrial gene organization, gene order and codon usage of the leech Whitmania pigra (Annelida), which is the first representative from the class Hirudinea. It is a circular molecule of 14,426bp, and encodes 13 protein-coding genes, 2 ribosomal RNA genes, and 22 transfer RNA genes. All 37 genes of W. pigra mitochondrial genome are transcribed from the same strand, which is identical to studied annelids, two echiurans, two sipunculans and many other lophotrochozoans. Five conserved gene clusters can be found in mitochondrial genomes of nine studied annelids, including (1) cox1-N-cox2; (2) cox3-Q-nad6-cob-W-atp6; (3) H-nad5-F-E-P-T-nad4L-nad4; (4) srRNA-V-lrRNA; and (5) nad3-S(1)-nad2. Compared with that of other studied annelids, translocations of transfer RNAs were found in the gene arrangement of W. pigra mitochondrial genome. Phylogenetic analysis strongly support that the species from Hirudinina and Oligochaeta form a monophyletic group Clitellata (BPM=100, BPP=100), which is consistent with previous research based on morphological and other molecular data. Both gene order data and amino acid sequences reveal that echiurans are derived annelids and sipunculans should be clustered with annelids and echiurans.     

Mitochondrial DNA in metazoa: degree of freedom in a frozen event

The mitochondrial genome (mtDNA), due to its peculiar features such as exclusive presence of orthologous genes, uniparental inheritance, lack of recombination, small size and constant gene content, certainly represents a major model system in studies on evolutionary genomics in metazoan. In 800 million years of evolution the gene content of metazoan mitochondrial genomes has remained practically frozen but several evolutionary processes have taken place. These processes, reviewed here, include rearrangements of gene order, changes in base composition and arising of compositional asymmetry between the two strands, variations in the genetic code and evolution of codon usage, lineage-specific nucleotide substitution rates and evolutionary patterns of mtDNA control regions.     

The Cephalopod Loligo bleekeri Mitochondrial Genome: Multiplied Noncoding Regions and Transposition of tRNA Genes

We previously reported the sequence of a 9260-bp fragment of mitochondrial (mt) DNA of the cephalopod Loligo bleekeri [J. Sasuga et al. (1999) J. Mol. Evol. 48:692–702]. To clarify further the characteristics of Loligo mtDNA, we have sequenced an 8148-bp fragment to reveal the complete mt genome sequence. Loligo mtDNA is 17,211 bp long and possesses a standard set of metazoan mt genes. Its gene arrangement is not identical to any other metazoan mt gene arrangement reported so far. Three of the 19 noncoding regions longer than 10 bp are 515, 507, and 509 bp long, and their sequences are nearly identical, suggesting that multiplication of these noncoding regions occurred in an ancestral Loligo mt genome. Comparison of the gene arrangements of Loligo, Katharina tunicata, and Littorina saxatilis mt genomes revealed that 17 tRNA genes of the Loligo mt genome are adjacent to noncoding regions. A majority (15 tRNA genes) of their counterparts is found in two tRNA gene clusters of the Katharina mt genome. Therefore, the Loligo mt genome (17 tRNA genes) may have spread over the genome, and this may have been coupled with the multiplication of the noncoding regions. Maximum likelihood analysis of mt protein genes supports the clade Mollusca + Annelida + Brachiopoda but fails to infer the relationships among Katharina, Loligo, and three gastropod species. Received: 9 May 2001 / Accepted: 3 October 2001     

Evolution of gastropod mitochondrial genome arrangements

Background  

Gastropod mitochondrial genomes exhibit an unusually great variety of gene orders compared to other metazoan mitochondrial genome such as e.g those of vertebrates. Hence, gastropod mitochondrial genomes constitute a good model system to study patterns, rates, and mechanisms of mitochondrial genome rearrangement. However, this kind of evolutionary comparative analysis requires a robust phylogenetic framework of the group under study, which has been elusive so far for gastropods in spite of the efforts carried out during the last two decades. Here, we report the complete nucleotide sequence of five mitochondrial genomes of gastropods (Pyramidella dolabrata, Ascobulla fragilis, Siphonaria pectinata, Onchidella celtica, and Myosotella myosotis), and we analyze them together with another ten complete mitochondrial genomes of gastropods currently available in molecular databases in order to reconstruct the phylogenetic relationships among the main lineages of gastropods.     

The mitochondrial genome of Phoronis architecta--comparisons demonstrate that phoronids are lophotrochozoan protostomes

The proper reconstruction of the relationships among the animal phyla is central to interpreting patterns of animal evolution from the genomic level to the morphological level. This is true not only of the more speciose phyla but also of smaller groups. We report here the nearly complete DNA sequence of the mitochondrial genome of the phoronid Phoronis architecta, which has a gene arrangement remarkably similar to that of a protostome animal, the chiton Katharina tunicata. Evolutionary analysis of both gene arrangements and inferred amino acid sequences of these taxa, along with those of three brachiopods and other diverse animals, strongly supports the hypothesis that lophophorates are part of the large group that includes mollusks and annelids-i.e., the Lophotrochozoa-and solidly refutes the alternative of their being deuterostomes.     

A multipartite mitochondrial genome in the potato cyst nematode Globodera pallida

The mitochondrial genome (mtDNA) of the plant parasitic nematode Globodera pallida exists as a population of small, circular DNAs that, taken individually, are of insufficient length to encode the typical metazoan mitochondrial gene complement. As far as we are aware, this unusual structural organization is unique among higher metazoans, although interesting comparisons can be made with the multipartite mitochondrial genome organizations of plants and fungi. The variation in frequency between populations displayed by some components of the mtDNA is likely to have major implications for the way in which mtDNA can be used in population and evolutionary genetic studies of G. pallida.     

The mitochondrial genome of the water spider Argyroneta aquatica (Araneae: Cybaeidae)

We sequenced nearly the entire mitochondrial genome of Argyroneta aquatica, a wholly underwater‐living spider, thereby enhancing the available genomic information for Arachnida. The confirmed sequences contained the complete set of known genes present in other metazoan mitochondrial genomes. However, the mitochondrial gene order of A. aquatica was distinctly different from that of the most distant Chelicerata Limulus polyphemus (Xiphosura), probably because of a series of gene translocations and/or inversions. Comparison of arachnid mitochondrial gene orders for the purpose of phylogenetic inference is only minimally useful, but provides a strong signal in closely related lineages. To test the basal relationships and the evolutionary pattern of tRNA gene rearrangements among Arachnida, phylogenetic analyses using amino acid sequences of the 13 protein‐coding genes were performed. An interesting feature, the five 135‐bp tandem repeats and two 363‐bp tandem repeats, was identified in the putative control region. Although control region tandem repeats have been reported in many other arachnid and metazoan species, this is the first time it has been described in spiders.     

What can the mitochondrial genome reveal about higher‐level phylogeny of the molluscan class Cephalopoda?

We present the first analysis of cephalopod mitochondrial gene order and construct phylogenies based on gene order using Bayesian, distance, and parsimony analysis methods. Analyses included all species of cephalopod for which the whole mitochondrial genome has been sequenced. Where resolution was obtained, these analyses supported division of Neocoleoidea, in which all recent coleoid Cephalopoda can be placed, into Octopodiformes and Decapodiformes. For the same taxa, we also constructed a phylogeny in a maximum likelihood framework based on amino‐acid coded sequence data of all mitochondrial protein coding genes. As well as supporting Octopodiformes and Decapodiformes, amino‐acid analyses established support for Teuthoidea (Oegospida and Myopsida) to the exclusion of Sepiidae, and supported a monophyletic Oegopsida. Partial mitochondrial sequences of additional higher‐level taxa for which whole genome data were not available were subsequently included in the amino‐acid analysis to provide additional information on phylogeny. Spirulida was found to be basal amongst Decapodiformes. Mapping of morphological characters onto our phylogeny and consideration of palaeontological evidence suggests that our phylogeny reflects true evolutionary relationships. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161 , 573–586.     

Nearly complete mitochondrial genome of Polyascus gregaria and the phylogenetic relationships among maxillopodans

We determined for the first time the nearly complete mitochondrial genome sequence of the entozoic Polyascus gregaria, a representative of Rhizocephala, Cirripedia. The nearly complete mitogenome was 15, 465 bp in length, consisting of 11 protein-coding genes, two rRNA genes, 22 tRNA genes and one major incomplete noncoding region. In total there are 73 overlapping nucleotides and 17 spacers between genes. All genes sequenced in P. gregaria mtDNA (including RNAs) were encoded on the same strand of the DNA, and the gene arrangement differed from that of other metazoan animals. The mitochondrial genome rearrangements included translocation of at least 8 genes and even inversion of the coding polarity of at least 2 genes. Comparative analysis of the gene orders with other maxillopodan mtDNAs showed that the unique characteristics of the thoracican cirripeds lineage were not observed in this representative of rhizocephalan. Phylogenetic analyses supported a close affinity of Rhizocephala to Thoracica. By adding the mitochondrial genomes from 4 copepods, the reciprocally monophyletic cirripeds and copepods clustered as sister groups, refusing the close relationship between Cirripedia and Remipedia. However, the monophyly of Maxillopoda was not supported in this study.     

Phylogeny and biogeography of highly diverged freshwater fish species (Leuciscinae,Cyprinidae, Teleostei) inferred from mitochondrial genome analysis

The distribution of freshwater taxa is a good biogeographic model to study pattern and process of vicariance and dispersal. The subfamily Leuciscinae (Cyprinidae, Teleostei) consists of many species distributed widely in Eurasia and North America. Leuciscinae have been divided into two phyletic groups, leuciscin and phoxinin. The phylogenetic relationships between major clades within the subfamily are poorly understood, largely because of the overwhelming diversity of the group. The origin of the Far Eastern phoxinin is an interesting question regarding the evolutionary history of Leuciscinae. Here we present phylogenetic analysis of 31 species of Leuciscinae and outgroups based on complete mitochondrial genome sequences to clarify the phylogenetic relationships and to infer the evolutionary history of the subfamily.     

Mitochondrial DNA variations and nuclear RFLPs reflect different genetic similarities among 23 Arabidopsis thaliana ecotypes

The mitochondrial genome of 23 Arabidopsis thaliana ecotypes was analysed by Southern hybridization in total cellular DNA. Firstly, the extent of divergence between the mitochondrial genomes in closely related lines of one plant species and secondly, the use of mitochondrial versus nuclear RFLPs to determine evolutionary relationships between Arabidopsis ecotype isolates was investigated. Highly divergent stoichiometries of alternative mitochondrial genome arrangements characterize individual ecotypes including the complete loss of a 5 kb region from ecotype Landsberg without apparent effect on plant viability. The genetic similarities between ecotypes suggested by mitochondrial genome arrangements differ from those deduced from 18 nuclear RFLP loci (CAPS markers). Similarity of nuclear RFLP patterns among the 23 Arabidopsis ecotypes neitehr correlates with their geographic origin nor with the observed mitochondrial genome arrangements. A promiscuous mitochondrial sequence insertion previously identified in ecotype Columbia is also found in the nuclear genomes of ecotypes Eifel, Enkheim and Hilversum. Two ecotypes (Eifel and Tabor) displaying identical RFLP patterns at all 18 nuclear loci show differences in both this sequence transfer and a mitochondrial DNA recombination event.