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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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Effective number of codons versus G+C content in third codon position in crustacean mitochondrial genes. All species with complete mitochondrial genome entries are included (for a species list, GenBank accession numbers and single values see supplementary Table 1). For each species eleven mitochondrial protein-coding genes were evaluated and plotted (all except nad4L and atp8, which contain less than 100 codons). Black dots: genes from Isopoda; orange dots: genes from all other Malacostraca; white dots: genes from Crustacea excl. Malacostraca. Regression line with r2 = 0.3381; p < 0.01.
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Figure 2: Effective number of codons versus G+C content in third codon position in crustacean mitochondrial genes. All species with complete mitochondrial genome entries are included (for a species list, GenBank accession numbers and single values see supplementary Table 1). For each species eleven mitochondrial protein-coding genes were evaluated and plotted (all except nad4L and atp8, which contain less than 100 codons). Black dots: genes from Isopoda; orange dots: genes from all other Malacostraca; white dots: genes from Crustacea excl. Malacostraca. Regression line with r2 = 0.3381; p < 0.01.

Mentions: The effective number of codons (ENC) is a statistic describing how far codon usage in protein-coding genes departs from the equal usage of all synonymous codons [40]. Its range lies between 20 (when only one codon is used for each amino acid) and 62 (when all synonymous codons are equally in use). The latter departs from the usual value of 61 for nuclear genes as in invertebrate mitochondrial genomes 62 codons are in use (instead being a stop codon, UGA codes for tryptophane in the invertebrate mitochondrial code). The ENC of all published crustacean mitochondrial genomes was determined for all genes (Fig. 2), except nad4L and atp8, because these genes are too short (less than 100 codons) to get proper results. A positive correlation with G+C content in third codon positions was revealed (r2 = 0.3381; p < 0.01). There is no obvious difference seen between malacostracan and other crustaceans. Genes from the two isopod species (Ligia oceanica and Idotea baltica) are of higher G+C content and therefore show a higher than average number of effective codons. For numbers of effective codons for individual species and genes, as well as GenBank accession numbers see additional file 1.


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)

Effective number of codons versus G+C content in third codon position in crustacean mitochondrial genes. All species with complete mitochondrial genome entries are included (for a species list, GenBank accession numbers and single values see supplementary Table 1). For each species eleven mitochondrial protein-coding genes were evaluated and plotted (all except nad4L and atp8, which contain less than 100 codons). Black dots: genes from Isopoda; orange dots: genes from all other Malacostraca; white dots: genes from Crustacea excl. Malacostraca. Regression line with r2 = 0.3381; p < 0.01.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Effective number of codons versus G+C content in third codon position in crustacean mitochondrial genes. All species with complete mitochondrial genome entries are included (for a species list, GenBank accession numbers and single values see supplementary Table 1). For each species eleven mitochondrial protein-coding genes were evaluated and plotted (all except nad4L and atp8, which contain less than 100 codons). Black dots: genes from Isopoda; orange dots: genes from all other Malacostraca; white dots: genes from Crustacea excl. Malacostraca. Regression line with r2 = 0.3381; p < 0.01.
Mentions: The effective number of codons (ENC) is a statistic describing how far codon usage in protein-coding genes departs from the equal usage of all synonymous codons [40]. Its range lies between 20 (when only one codon is used for each amino acid) and 62 (when all synonymous codons are equally in use). The latter departs from the usual value of 61 for nuclear genes as in invertebrate mitochondrial genomes 62 codons are in use (instead being a stop codon, UGA codes for tryptophane in the invertebrate mitochondrial code). The ENC of all published crustacean mitochondrial genomes was determined for all genes (Fig. 2), except nad4L and atp8, because these genes are too short (less than 100 codons) to get proper results. A positive correlation with G+C content in third codon positions was revealed (r2 = 0.3381; p < 0.01). There is no obvious difference seen between malacostracan and other crustaceans. Genes from the two isopod species (Ligia oceanica and Idotea baltica) are of higher G+C content and therefore show a higher than average number of effective codons. For numbers of effective codons for individual species and genes, as well as GenBank accession numbers see additional file 1.

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
Related in: MedlinePlus