Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-24T02:45:13.594Z Has data issue: false hasContentIssue false

Structure and organization of the mitochondrial genome of the canine heartworm, Dirofilaria immitis

Published online by Cambridge University Press:  09 October 2003

M. HU
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
R. B. GASSER
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
Y. G. ABS EL-OSTA
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
N. B. CHILTON
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia

Abstract

This study determined the complete mitochondrial (mt) genome sequence of the canine heartworm, Dirofilaria immitisThe complete nucleotide sequence for the mitochondrial genome of Dirofilaria immitis is available from the EMBL database under the Accession Number AJ537512., and compared its structure, organization and other characteristics with Onchocerca volvulus and other secernentean nematodes. The D. immitis mt genome is 13814 bp in size and contains 36 of the 37 genes typical of metazoan organisms, and lacks the ATP synthetase subunit 8 gene. All of the genes are transcribed in the same direction. For the entire genome, the nucleotide contents are ∼55% (T), ∼19% (each for A and G) and ∼7% (C), which is very similar to those of the protein-coding genes. In the latter genes, most (∼69%) third codon positions have a T, but rarely (∼1–9%) have an A or a C. The C content (8–12%) is higher at the first and second codon positions compared with the third position (∼1%). These nucleotide biases have a significant effect on the codon usage patterns and, thus, on the amino acid composition of the proteins. The mt genome organization of D. immitis is essentially the same as that of O. volvulus, but is distinctly different from other secernentean nematodes sequenced thus far. Irrespective of transpositions of transfer RNA (trn) genes and the non-coding, AT-rich region, there are 4 gene- or gene block-translocations between the mt genome of D. immitis and those of Caenorhabditis elegans, Ascaris suum and the 2 human hookworms, Ancylostoma duodenale and Necator americanus. For D. immitis, the 22 trn genes have secondary structures typical of other secernentean nematodes, and possess a TV-replacement loop instead of a TΨC arm and loop. Like O. volvulus, the mt trnK and trnP of D. immitis use the anticodons CUU and AGG, whereas in other nematodes, UUU and UGG are employed, respectively. Also, the secondary structures of the 2 ribosomal RNA (rrn) genes are similar to the models for other nematodes. Overall, the availability of the complete D. immitis mt genome sequence provides a resource for future studies of the comparative mt genomics and of the population genetics and/or phylogeny of parasitic nematodes.

Type
Research Article
Copyright
2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ASAKAWA, S., KUMAZAWA, Y., ARAKI, T., HIMERO, H., MIURA, K. & WATANABE, K. (1991). Strand specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. Journal of Molecular Evolution 32, 511520.CrossRefGoogle Scholar
BEAGLEY, C. T., OKIMOTO, R. & WOLSTENHOLME, D. R. (1999). Mytilus mitochondrial DNA contains a functional gene for a tRNAser(UCN) with a dihydrouridine arm-replacement loop and a pseudo- tRNAser(UCN) gene. Genetics 152, 641652.Google Scholar
BLACK, W. C. 4TH & ROEHRDANZ, R. L. (1998). Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. Molecular Biology and Evolution 15, 17721785.CrossRefGoogle Scholar
BOORE, J. L. (1999). Animal mitochondrial genomes. Nucleic Acids Research 27, 17671780.CrossRefGoogle Scholar
BOORE, J. L. & BROWN, W. M. (1994). Complete DNA sequence of the mitochondrial genome of the black chiton, Katharina tunicata. Genetics 138, 423443.Google Scholar
BOORE, J. L. & BROWN, W. M. (1995). Complete sequence of the mitochondrial DNA of the annelid worm Lumbricus terrestris. Genetics 141, 305319.Google Scholar
BOWLES, J., BLAIR, D. & McMANUS, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165173.CrossRefGoogle Scholar
CAMPBELL, N. J. H. & BARKER, S. C. (1999). The novel mitochondrial gene arrangement of the cattle tick, Boophilus microplus: fivefold tandem repetition of a coding region. Molecular Biology and Evolution 16, 732740.CrossRefGoogle Scholar
CASTRESANA, J., FELDMAIER-FUCHS, G. & PÄÄBO, S. (1998). Codon reassignment and amino acid composition in hemichordate mitochondria. Proceedings of the National Academy of Sciences, USA 95, 37033707.CrossRefGoogle Scholar
CRINGOLI, G., RINALDI, L., VENEZIANO, V. & CAPELLI, G. (2001). A prevalence survey and risk analysis of filariosis in dogs from the Mt. Vesuvius of southern Italy. Veterinary Parasitology 102, 243252.Google Scholar
DOWTON, M. & CAMPBELL, N. J. H. (2001). Intramitochondrial recombination – is it why some mitochondrial genes sleep around? Trends in Ecology and Evolution 16, 269271.Google Scholar
DOWTON, M., CASTRO, L. R. & AUSTIN, A. D. (2002). Mitochondrial gene rearrangements as phylogenetic characters in the invertebrates: the examination of genome ‘morphology’. Invertebrate Systematics 16, 345356.CrossRefGoogle Scholar
FAN, C.-K., SU, K.-E., LIN, Y.-H., LIAO, C.-W., DU, W.-Y. & CHIOU, H.-Y. (2001). Seroepidemiologic survey of Dirofilaria immitis infection among domestic dogs in Taipei city and mountain aboriginal districts in Taiwan (1998–1999). Veterinary Parasitology 102, 113120.CrossRefGoogle Scholar
GASSER, R. B., CHILTON, N. B., HOSTE, H. & BEVERIDGE, I. (1993). Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 25252526.CrossRefGoogle Scholar
GIORGI, C. E., MARTIRADONNA, A., LANAVE, C. & SACCONE, C. (1996). Complete sequence of the mitochondrial DNA in the sea urchin Arbacia lixula: conserved features of the echinoid mitochondrial genome. Molecular Phylogenetics and Evolution 5, 323332.CrossRefGoogle Scholar
HOFFMANN, R. J., BOORE, J. L. & BROWN, W. M. (1992). A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131, 397412.Google Scholar
HU, M., CHILTON, N. B. & GASSER, R. B. (2002). The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: Secernentea). International Journal for Parasitology 32, 145158.CrossRefGoogle Scholar
KEDDIE, E. M., HIGAZI, T. & UNNASCH, T. R. ( 1998). The mitochondrial genome of Onchocerca volvulus: sequence, structure and phylogenetic analysis. Molecular and Biochemical Parasitology 95, 111127.CrossRefGoogle Scholar
LAVROV, D. V. & BROWN, W. M. ( 2001). Trichinella spiralis mtDNA: a nematode mitochondrial genome that encodes a putative ATP8 and normally structured tRNAs and has a gene arrangement relatable to those of coelomate metazoans. Genetics 157, 621637.Google Scholar
LAVROV, D. V., BROWN, W. M. & BOORE, J. L. ( 2000). A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proceedings of the National Academy of Sciences, USA 97, 1373813742.CrossRefGoogle Scholar
LE, T. H., BLAIR, D., AGATSUMA, T., HUMAIR, P.-F., CAMPBELL, N. J. H., IWAGAMI, M., LITTLEWOOD, D. T. J., PEACOCK, B., JOHNSTON, D. A., BARTLEY, J., ROLLINSON, D., HERNIOU, E. A., ZARLENGA, D. S. & McMANUS, D. P. ( 2000). Phylogenies inferred from mitochondrial gene orders – a cautionary tale from the parasitic flatworms. Molecular Biology and Evolution 17, 11231125.CrossRefGoogle Scholar
LE, T. H., BLAIR, D. & McMANUS, D. P. (2000). Mitochondrial genomes of human helminths and their use as markers in population genetics and phylogeny. Acta Tropica 77, 243256.CrossRefGoogle Scholar
LE, T. H., BLAIR, D. & McMANUS, D. P. (2001). Complete DNA sequence and gene organization of the mitochondrial genome of the liverfluke, Fasciola hepatica L. (Platyhelminthes, Trematoda). Parasitology 123, 609621.Google Scholar
LE, T. H., BLAIR, D. & McMANUS, D. P. (2002). Mitochondrial genomes of parasitic flatworms. Trends in Parasitology 18, 206213.CrossRefGoogle Scholar
LOWE, T. M. & EDDY, S. R. (1997). tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research 25, 955964.CrossRefGoogle Scholar
LUNT, D. H. & HYMAN, B. C. (1997). Animal mitochondrial DNA recombination. Nature, London 387, 247.CrossRefGoogle Scholar
MACEY, J. R., LARSON, A., ANANJEVA, N. B., FANG, Z. & PAPENFUSS, T. J. (1997). Two novel gene orders and the role of light-strand replication in arrangement of the vertebrate mitochondrial genome. Molecular Biology and Evolution 14, 91104.CrossRefGoogle Scholar
MAR, P. H., YANG, I.-C., CHANG, G.-N. & FEI, A. C.-Y. (2002). Specific polymerase chain reaction for differential diagnosis of Dirofilaria immitis and Dipetalonema reconditum using primers derived from internal transcribed spacer region 2 (ITS2). Veterinary Parasitology 106, 243252.CrossRefGoogle Scholar
MORITZ, C., DOWLING, T. E. & BROWN, W. M. (1987). Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annual Review of Ecology and Systematics 18, 269292.CrossRefGoogle Scholar
von NICKISCH-ROSENEGK, M., BROWN, W. N. & BOORE, J. L. (2001). Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate the platyhelminths are eutrochozoans. Molecular Biology and Evolution 18, 721730.CrossRefGoogle Scholar
OHTSUKI, T., SATO, A., WATANABE, Y.-I. & WATANABE, K. (2002). A unique serine-specific elongation factor Tu found in nematode mitochondria. Nature, Structural Biology 9, 669673.CrossRefGoogle Scholar
OHTSUKI, T., WATANABE, Y.-I., TAKEMOTO, C., KAWAI, G., UEDA, T., KITA, K., KOJIMA, S., KAZIRO, Y., NYBORG, J. & WATANABE, K. (2001). An ‘elongated’ translation factor Tu for truncated tRNAs in nematode mitochondria. Journal of Biological Biochemistry 276, 2157121577.CrossRefGoogle Scholar
OJALA, D., MONTAYA, J. & ATTARDI, G. (1981). tRNA punctuation model of RNA processing in human mitochondria. Nature, London 290, 470474.CrossRefGoogle Scholar
OKIMOTO, R., MACFARLANE, J. L., CLARY, D. O. & WOLSTENHOLME, D. R. (1992). The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130, 471498.Google Scholar
RAWLINGS, T. A., COLLINE, T. M. & BIELER, R. (2001). A major mitochondrial gene rearrangement among closely related species. Molecular Biology and Evolution 18, 16041609.CrossRefGoogle Scholar
SACCONE, C., DE GIORGI, C., GISSI, C., PESOLE, G. & REYES, A. (1999). Evolutionary genomics in metazoa: the mitochondrial DNA as a model system. Gene 238, 195209.CrossRefGoogle Scholar
SANTALUCIA, J. (1998). A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proceedings of the National Academy of Sciences, USA 95, 14601465.CrossRefGoogle Scholar
SHADEL, G. S. & CLAYTON, D. A. (1997). Mitochondrial DNA maintenance in vertebrates. Annual Review of Biochemistry 66, 409435.CrossRefGoogle Scholar
SHARP, P. M. & MATASSI, G. (1994). Codon usage and genome evolution. Current Opinions of Genetic Development 4, 851860.CrossRefGoogle Scholar
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINA, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.CrossRefGoogle Scholar
UNNASCH, T. R. (2002). River blindness. Lancet 360, 182183.CrossRefGoogle Scholar
WOLSTENHOLME, D. R., MACFARLANE, J. L., OKIMOTO, R., CLARY, D. O. & WAHLEITHNER, J. A. (1987). Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proceedings of the National Academy of Sciences, USA 84, 13241328.CrossRefGoogle Scholar
WOLSTENHOLME, D. R. (1992). Animal mitochondrial DNA: structure and evolution. International Review of Cytology 141, 173216.CrossRefGoogle Scholar
WOLSTENHOLME, D. R., OKIMOTO, R. & MACFARLANE, J. L. (1994). Nucleotide correlations that suggest tertiary interactions in the TV-replacement loop-containing mitochondrial tRNAs of the nematodes, Caenorhabditis elegans and Ascaris suum. Nucleic Acids Research 22, 43004306.CrossRefGoogle Scholar
YOKOBORI, S.-I. & PÄÄBO, S. (1995). tRNA editing in metazoans. Nature, London 377, 490.CrossRefGoogle Scholar
YOKOBORI, S.-I. & PÄÄBO, S. (1997). Polyadenylation creates the discriminator nucleotide of chicken mitochondrial tRNA (Tyr). Journal of Molecular Biology 265, 9599.CrossRefGoogle Scholar