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The complete mitochondrial genome of the common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and unusual control region features.

Kilpert F, Podsiadlowski L - BMC Genomics (2006)

Bottom Line: It shows several changes in mitochondrial gene order compared to other crustacean species.The two isopod species Ligia oceanica and Idotea baltica show a similarly derived gene order, compared to the arthropod ground pattern and to the amphipod Parhyale hawaiiensis, suggesting that most of the translocation events were already present the last common ancestor of these isopods.This is probably due to a reversal of the replication origin, which is further supported by the fact that the hairpin structure typically found in the control region shows a reversed orientation in the isopod species, compared to other crustaceans.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Animal Systematics and Evolution, Institute of Biology, Freie Universit├Ąt Berlin, Konigin-Luise-Str, 1-3, D-14195 Berlin, Germany. fkil@zedat.fu-berlin.de

ABSTRACT

Background: Sequence data and other characters from mitochondrial genomes (gene translocations, secondary structure of RNA molecules) are useful in phylogenetic studies among metazoan animals from population to phylum level. Moreover, the comparison of complete mitochondrial sequences gives valuable information about the evolution of small genomes, e.g. about different mechanisms of gene translocation, gene duplication and gene loss, or concerning nucleotide frequency biases. The Peracarida (gammarids, isopods, etc.) comprise about 21,000 species of crustaceans, living in many environments from deep sea floor to arid terrestrial habitats. Ligia oceanica is a terrestrial isopod living at rocky seashores of the european North Sea and Atlantic coastlines.

Results: The study reveals the first complete mitochondrial DNA sequence from a peracarid crustacean. The mitochondrial genome of Ligia oceanica is a circular double-stranded DNA molecule, with a size of 15,289 bp. It shows several changes in mitochondrial gene order compared to other crustacean species. An overview about mitochondrial gene order of all crustacean taxa yet sequenced is also presented. The largest non-coding part (the putative mitochondrial control region) of the mitochondrial genome of Ligia oceanica is unexpectedly not AT-rich compared to the remainder of the genome. It bears two repeat regions (4x 10 bp and 3x 64 bp), and a GC-rich hairpin-like secondary structure. Some of the transfer RNAs show secondary structures which derive from the usual cloverleaf pattern. While some tRNA genes are putative targets for RNA editing, trnR could not be localized at all.

Conclusion: Gene order is not conserved among Peracarida, not even among isopods. The two isopod species Ligia oceanica and Idotea baltica show a similarly derived gene order, compared to the arthropod ground pattern and to the amphipod Parhyale hawaiiensis, suggesting that most of the translocation events were already present the last common ancestor of these isopods. Beyond that, the positions of three tRNA genes differ in the two isopod species. Strand bias in nucleotide frequency is reversed in both isopod species compared to other Malacostraca. This is probably due to a reversal of the replication origin, which is further supported by the fact that the hairpin structure typically found in the control region shows a reversed orientation in the isopod species, compared to other crustaceans.

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Phylogenetic tree of Malacostraca. Only those species with GenBank entries for complete or almost complete mitochondrial genomes are included. Hypotheses of gene translocation events are mapped to the corresponding clades (numbers correspond to those in Fig. 8). Due to the uncertain homology, translocations of the major non-coding region were not considered. Phylogeny according to [77].
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Figure 9: Phylogenetic tree of Malacostraca. Only those species with GenBank entries for complete or almost complete mitochondrial genomes are included. Hypotheses of gene translocation events are mapped to the corresponding clades (numbers correspond to those in Fig. 8). Due to the uncertain homology, translocations of the major non-coding region were not considered. Phylogeny according to [77].

Mentions: Among Malacostraca 10 from 19 species have retained the pancrustacean ground pattern: six mantis shrimps (Stomatopoda) and four members of Decapoda (Fig. 8 and 9). Among Decapoda independent translocation events changed gene order in Pagurus longicarpus [66], Cherax destructor [33], and Brachyura. The four species of Brachyura share a translocation of trnH, the freshwater crabs Geothelphusa dehaani [67] and Eriocheir japonica [68] show further translocations. In the Euphausiacea Euphausia superba a swap between trnL1 and trnL2 seems to have happened, probably preceded by a gene duplication [43].


The complete mitochondrial genome of the common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and unusual control region features.

Kilpert F, Podsiadlowski L - BMC Genomics (2006)

Phylogenetic tree of Malacostraca. Only those species with GenBank entries for complete or almost complete mitochondrial genomes are included. Hypotheses of gene translocation events are mapped to the corresponding clades (numbers correspond to those in Fig. 8). Due to the uncertain homology, translocations of the major non-coding region were not considered. Phylogeny according to [77].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1590035&req=5

Figure 9: Phylogenetic tree of Malacostraca. Only those species with GenBank entries for complete or almost complete mitochondrial genomes are included. Hypotheses of gene translocation events are mapped to the corresponding clades (numbers correspond to those in Fig. 8). Due to the uncertain homology, translocations of the major non-coding region were not considered. Phylogeny according to [77].
Mentions: Among Malacostraca 10 from 19 species have retained the pancrustacean ground pattern: six mantis shrimps (Stomatopoda) and four members of Decapoda (Fig. 8 and 9). Among Decapoda independent translocation events changed gene order in Pagurus longicarpus [66], Cherax destructor [33], and Brachyura. The four species of Brachyura share a translocation of trnH, the freshwater crabs Geothelphusa dehaani [67] and Eriocheir japonica [68] show further translocations. In the Euphausiacea Euphausia superba a swap between trnL1 and trnL2 seems to have happened, probably preceded by a gene duplication [43].

Bottom Line: It shows several changes in mitochondrial gene order compared to other crustacean species.The two isopod species Ligia oceanica and Idotea baltica show a similarly derived gene order, compared to the arthropod ground pattern and to the amphipod Parhyale hawaiiensis, suggesting that most of the translocation events were already present the last common ancestor of these isopods.This is probably due to a reversal of the replication origin, which is further supported by the fact that the hairpin structure typically found in the control region shows a reversed orientation in the isopod species, compared to other crustaceans.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Animal Systematics and Evolution, Institute of Biology, Freie Universit├Ąt Berlin, Konigin-Luise-Str, 1-3, D-14195 Berlin, Germany. fkil@zedat.fu-berlin.de

ABSTRACT

Background: Sequence data and other characters from mitochondrial genomes (gene translocations, secondary structure of RNA molecules) are useful in phylogenetic studies among metazoan animals from population to phylum level. Moreover, the comparison of complete mitochondrial sequences gives valuable information about the evolution of small genomes, e.g. about different mechanisms of gene translocation, gene duplication and gene loss, or concerning nucleotide frequency biases. The Peracarida (gammarids, isopods, etc.) comprise about 21,000 species of crustaceans, living in many environments from deep sea floor to arid terrestrial habitats. Ligia oceanica is a terrestrial isopod living at rocky seashores of the european North Sea and Atlantic coastlines.

Results: The study reveals the first complete mitochondrial DNA sequence from a peracarid crustacean. The mitochondrial genome of Ligia oceanica is a circular double-stranded DNA molecule, with a size of 15,289 bp. It shows several changes in mitochondrial gene order compared to other crustacean species. An overview about mitochondrial gene order of all crustacean taxa yet sequenced is also presented. The largest non-coding part (the putative mitochondrial control region) of the mitochondrial genome of Ligia oceanica is unexpectedly not AT-rich compared to the remainder of the genome. It bears two repeat regions (4x 10 bp and 3x 64 bp), and a GC-rich hairpin-like secondary structure. Some of the transfer RNAs show secondary structures which derive from the usual cloverleaf pattern. While some tRNA genes are putative targets for RNA editing, trnR could not be localized at all.

Conclusion: Gene order is not conserved among Peracarida, not even among isopods. The two isopod species Ligia oceanica and Idotea baltica show a similarly derived gene order, compared to the arthropod ground pattern and to the amphipod Parhyale hawaiiensis, suggesting that most of the translocation events were already present the last common ancestor of these isopods. Beyond that, the positions of three tRNA genes differ in the two isopod species. Strand bias in nucleotide frequency is reversed in both isopod species compared to other Malacostraca. This is probably due to a reversal of the replication origin, which is further supported by the fact that the hairpin structure typically found in the control region shows a reversed orientation in the isopod species, compared to other crustaceans.

Show MeSH