The Mitochondrial Genomes of Two Nematodes, Caenorhabditis elegans and Ascaris suum

INVESTIGATIONS

The Mitochondrial Genomes of Two Nematodes, Caenorhabditis elegans and Ascaris suum

R. Okimoto, J. L. Macfarlane, D. O. Clary and D. R. Wolstenholme
Department of Biology, University of Utah, Salt Lake City, Utah 84112

The nucleotide sequences of the mitochondrial DNA (mtDNA) molecules of two nematodes, Caenorhabditis elegans [13,794 nucleotide pairs (ntp)], and Ascaris suum (14,284 ntp) are presented and compared. Each molecule contains the genes for two ribosomal RNAs (s-rRNA and l-rRNA), 22 transfer RNAs (tRNAs) and 12 proteins, all of which are transcribed in the same direction. The protein genes are the same as 12 of the 13 protein genes found in other metazoan mtDNAs: Cyt b, cytochrome b; COI-III, cytochrome c oxidase subunits I-III; ATPase6, F(o) ATPase subunit 6; ND1-6 and 4L, NADH dehydrogenase subunits 1-6 and 4L: a gene for ATPase subunit 8, common to other metazoan mtDNAs, has not been identified in nematode mtDNAs. The C. elegans and A. suum mtDNA molecules both include an apparently noncoding sequence that contains runs of AT dinucleotides, and direct and inverted repeats (the AT region: 466 and 886 ntp, respectively). A second, apparently noncoding sequence in the C. elegans and A. suum mtDNA molecules (109 and 117 ntp, respectively) includes a single, hairpin-forming structure. There are only 38 and 89 other intergenic nucleotides in the C. elegans and A. suum mtDNAs, and no introns. Gene arrangements are identical in the C. elegans and A. suum mtDNA molecules except that the AT regions have different relative locations. However, the arrangement of genes in the two nematode mtDNAs differs extensively from gene arrangements in all other sequenced metazoan mtDNAs. Unusual features regarding nematode mitochondrial tRNA genes and mitochondrial protein gene initiation codons, previously described by us, are reviewed. In the C. elegans and A. suum mt-genetic codes, AGA and AGG specify serine, TGA specifies tryptophan and ATA specifies methionine. From considerations of amino acid and nucleotide sequence similarities it appears likely that the C. elegans and A. suum ancestral lines diverged close to the time of divergence of the cow and human ancestral lines, about 80 million years ago.

This article has been cited by other articles:

S. E. Masta and J. L. Boore
Parallel Evolution of Truncated Transfer RNA Genes in Arachnid Mitochondrial Genomes
Mol. Biol. Evol., May 1, 2008; 25(5): 949 - 959.
[Abstract] [Full Text] [PDF]

M. Arita, T. Suematsu, A. Osanai, T. Inaba, H. Kamiya, K. Kita, M. Sisido, Y.-i. Watanabe, and T. Ohtsuki
An evolutionary 'intermediate state' of mitochondrial translation systems found in Trichinella species of parasitic nematodes: co-evolution of tRNA and EF-Tu
Nucleic Acids Res., October 6, 2006; 34(18): 5291 - 5299.
[Abstract] [Full Text] [PDF]

Y. Valles and J. L. Boore
Lophotrochozoan mitochondrial genomes
Integr. Comp. Biol., August 1, 2006; 46(4): 544 - 557.
[Abstract] [Full Text] [PDF]

T. Suematsu, A. Sato, M. Sakurai, K. Watanabe, and T. Ohtsuki
A unique tRNA recognition mechanism of Caenorhabditis elegans mitochondrial EF-Tu2
Nucleic Acids Res., August 19, 2005; 33(15): 4683 - 4691.
[Abstract] [Full Text] [PDF]

A. Mizi, E. Zouros, N. Moschonas, and G. C. Rodakis
The Complete Maternal and Paternal Mitochondrial Genomes of the Mediterranean Mussel Mytilus galloprovincialis: Implications for the Doubly Uniparental Inheritance Mode of mtDNA
Mol. Biol. Evol., April 1, 2005; 22(4): 952 - 967.
[Abstract] [Full Text] [PDF]

M. Sakurai, T. Ohtsuki, and K. Watanabe
Modification at position 9 with 1-methyladenosine is crucial for structure and function of nematode mitochondrial tRNAs lacking the entire T-arm
Nucleic Acids Res., March 21, 2005; 33(5): 1653 - 1661.
[Abstract] [Full Text] [PDF]

S. P. Curran, E. P. Leverich, C. M. Koehler, and P. L. Larsen
Defective Mitochondrial Protein Translocation Precludes Normal Caenorhabditis elegans Development
J. Biol. Chem., December 24, 2004; 279(52): 54655 - 54662.
[Abstract] [Full Text] [PDF]

J. L. Boore, M. Medina, and L. A. Rosenberg
Complete Sequences of the Highly Rearranged Molluscan Mitochondrial Genomes of the Scaphopod Graptacme eborea and the Bivalve Mytilus edulis
Mol. Biol. Evol., August 1, 2004; 21(8): 1492 - 1503.
[Abstract] [Full Text] [PDF]

K. G. Helfenbein, H. M. Fourcade, R. G. Vanjani, and J. L. Boore
The mitochondrial genome of Paraspadella gotoi is highly reduced and reveals that chaetognaths are a sister group to protostomes
PNAS, July 20, 2004; 101(29): 10639 - 10643.
[Abstract] [Full Text] [PDF]

L. Cao, E. Kenchington, E. Zouros, and G. C. Rodakis
Evidence That the Large Noncoding Sequence Is the Main Control Region of Maternally and Paternally Transmitted Mitochondrial Genomes of the Marine Mussel (Mytilus spp.)
Genetics, June 1, 2004; 167(2): 835 - 850.
[Abstract] [Full Text] [PDF]

L. I. Grad and B. D. Lemire
Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis
Hum. Mol. Genet., February 1, 2004; 13(3): 303 - 314.
[Abstract] [Full Text] [PDF]

D. R. Denver, K. Morris, and W. K. Thomas
Phylogenetics in Caenorhabditis elegans: An Analysis of Divergence and Outcrossing
Mol. Biol. Evol., March 1, 2003; 20(3): 393 - 400.
[Abstract] [Full Text] [PDF]

T. Ohtsuki, M. Sakurai, A. Sato, and K. Watanabe
Characterization of the interaction between the nucleotide exchange factor EF-Ts from nematode mitochondria and elongation factor Tu
Nucleic Acids Res., December 15, 2002; 30(24): 5444 - 5451.
[Abstract] [Full Text] [PDF]

J. L. Boore and J. L. Staton
The Mitochondrial Genome of the Sipunculid Phascolopsis gouldii Supports Its Association with Annelida Rather than Mollusca
Mol. Biol. Evol., February 1, 2002; 19(2): 127 - 137.
[Abstract] [Full Text] [PDF]

V. Leignel and J.-F. Humbert
Mitochondrial DNA Variation in Benzimidazole-Resistant and -Susceptible Populations of the Small Ruminant Parasite Teladorsagia circumcincta
J. Hered., November 1, 2001; 92(6): 503 - 506.
[Abstract] [Full Text] [PDF]

K. G. Helfenbein, W. M. Brown, and J. L. Boore
The Complete Mitochondrial Genome of the Articulate Brachiopod Terebratalia transversa
Mol. Biol. Evol., September 1, 2001; 18(9): 1734 - 1744.
[Abstract] [Full Text] [PDF]

D. V. Lavrov and W. M. Brown
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, February 1, 2001; 157(2): 621 - 637.
[Abstract] [Full Text]

D. R. Denver, K. Morris, M. Lynch, L. L. Vassilieva, and W. K. Thomas
High Direct Estimate of the Mutation Rate in the Mitochondrial Genome of Caenorhabditis elegans
Science, September 29, 2000; 289(5488): 2342 - 2344.
[Abstract] [Full Text]

Y. Noguchi, K. Endo, F. Tajima, and R. Ueshima
The Mitochondrial Genome of the Brachiopod Laqueus rubellus
Genetics, May 1, 2000; 155(1): 245 - 259.
[Abstract] [Full Text]

M. R. Armstrong, V. C. Blok, and M. S. Phillips
A Multipartite Mitochondrial Genome in the Potato Cyst Nematode Globodera pallida
Genetics, January 1, 2000; 154(1): 181 - 192.
[Abstract] [Full Text]

S.-i. Yokobori, T. Ueda, G. Feldmaier-Fuchs, S. Pääbo, R. Ueshima, A. Kondow, K. Nishikawa, and K. Watanabe
Complete DNA Sequence of the Mitochondrial Genome of the Ascidian Halocynthia roretzi (Chordata, Urochordata)
Genetics, December 1, 1999; 153(4): 1851 - 1862.
[Abstract] [Full Text]

K. K. A. Tetteh, A. Loukas, C. Tripp, and R. M. Maizels
Identification of Abundantly Expressed Novel and Conserved Genes from the Infective Larval Stage of Toxocara canis by an Expressed Sequence Tag Strategy
Infect. Immun., September 1, 1999; 67(9): 4771 - 4779.
[Abstract] [Full Text] [PDF]

C. T. Beagley, R. Okimoto, and D. R. Wolstenholme
Mytilus Mitochondrial DNA Contains a Functional Gene for a tRNASer(UCN) With a Dihydrouridine Arm-Replacement Loop and a pseudo-tRNASer(UCN) Gene
Genetics, June 1, 1999; 152(2): 641 - 652.
[Abstract] [Full Text]

The C. elegans Sequencing Consortium
Genome Sequence of the Nematode C. elegans: A Platform for Investigating Biology
Science, December 11, 1998; 282(5396): 2012 - 2018.
[Abstract] [Full Text]

J. Castresana, G. Feldmaier-Fuchs, and S. Paabo
Codon reassignment and amino acid composition in hemichordate mitochondria
PNAS, March 31, 1998; 95(7): 3703 - 3707.
[Abstract] [Full Text] [PDF]

C. T. Beagley, R. Okimoto, and D. R. Wolstenholme
The Mitochondrial Genome of the Sea Anemone Metridium senile (Cnidaria): Introns, a Paucity of tRNA Genes, and a Near-Standard Genetic Code
Genetics, March 1, 1998; 148(3): 1091 - 1108.
[Abstract] [Full Text] [PDF]

S. Matsuyama, T. Ueda, P. F. Crain, J. A. McCloskey, and K. Watanabe
A Novel Wobble Rule Found in Starfish Mitochondria. PRESENCE OF 7-METHYLGUANOSINE AT THE ANTICODON WOBBLE POSITION EXPANDS DECODING CAPABILITY OF tRNA
J. Biol. Chem., February 6, 1998; 273(6): 3363 - 3368.
[Abstract] [Full Text] [PDF]

T. Ohtsuki, Y.-i. Watanabe, C. Takemoto, G. Kawai, T. Ueda, K. Kita, S. Kojima, Y. Kaziro, J. Nyborg, and K. Watanabe
An "Elongated" Translation Elongation Factor Tu for Truncated tRNAs in Nematode Mitochondria
J. Biol. Chem., June 8, 2001; 276(24): 21571 - 21577.
[Abstract] [Full Text] [PDF]

W. Y. Tsang, L. C. Sayles, L. I. Grad, D. B. Pilgrim, and B. D. Lemire
Mitochondrial Respiratory Chain Deficiency in Caenorhabditis elegans Results in Developmental Arrest and Increased Life Span
J. Biol. Chem., August 17, 2001; 276(34): 32240 - 32246.
[Abstract] [Full Text] [PDF]

S. J.M. Jones, D. L. Riddle, A. T. Pouzyrev, V. E. Velculescu, L. Hillier, S. R. Eddy, S. L. Stricklin, D. L. Baillie, R. Waterston, and M. A. Marra
Changes in Gene Expression Associated with Developmental Arrest and Longevity in Caenorhabditis elegans
Genome Res., August 1, 2001; 11(8): 1346 - 1352.
[Abstract] [Full Text] [PDF]

				M. Arita, T. Suematsu, A. Osanai, T. Inaba, H. Kamiya, K. Kita, M. Sisido, Y.-i. Watanabe, and T. Ohtsuki An evolutionary 'intermediate state' of mitochondrial translation systems found in Trichinella species of parasitic nematodes: co-evolution of tRNA and EF-Tu Nucleic Acids Res., October 6, 2006; 34(18): 5291 - 5299. [Abstract] [Full Text] [PDF]

				Y. Valles and J. L. Boore Lophotrochozoan mitochondrial genomes Integr. Comp. Biol., August 1, 2006; 46(4): 544 - 557. [Abstract] [Full Text] [PDF]

				T. Suematsu, A. Sato, M. Sakurai, K. Watanabe, and T. Ohtsuki A unique tRNA recognition mechanism of Caenorhabditis elegans mitochondrial EF-Tu2 Nucleic Acids Res., August 19, 2005; 33(15): 4683 - 4691. [Abstract] [Full Text] [PDF]

				A. Mizi, E. Zouros, N. Moschonas, and G. C. Rodakis The Complete Maternal and Paternal Mitochondrial Genomes of the Mediterranean Mussel Mytilus galloprovincialis: Implications for the Doubly Uniparental Inheritance Mode of mtDNA Mol. Biol. Evol., April 1, 2005; 22(4): 952 - 967. [Abstract] [Full Text] [PDF]

				M. Sakurai, T. Ohtsuki, and K. Watanabe Modification at position 9 with 1-methyladenosine is crucial for structure and function of nematode mitochondrial tRNAs lacking the entire T-arm Nucleic Acids Res., March 21, 2005; 33(5): 1653 - 1661. [Abstract] [Full Text] [PDF]

				S. P. Curran, E. P. Leverich, C. M. Koehler, and P. L. Larsen Defective Mitochondrial Protein Translocation Precludes Normal Caenorhabditis elegans Development J. Biol. Chem., December 24, 2004; 279(52): 54655 - 54662. [Abstract] [Full Text] [PDF]

				J. L. Boore, M. Medina, and L. A. Rosenberg Complete Sequences of the Highly Rearranged Molluscan Mitochondrial Genomes of the Scaphopod Graptacme eborea and the Bivalve Mytilus edulis Mol. Biol. Evol., August 1, 2004; 21(8): 1492 - 1503. [Abstract] [Full Text] [PDF]

				K. G. Helfenbein, H. M. Fourcade, R. G. Vanjani, and J. L. Boore The mitochondrial genome of Paraspadella gotoi is highly reduced and reveals that chaetognaths are a sister group to protostomes PNAS, July 20, 2004; 101(29): 10639 - 10643. [Abstract] [Full Text] [PDF]

				L. Cao, E. Kenchington, E. Zouros, and G. C. Rodakis Evidence That the Large Noncoding Sequence Is the Main Control Region of Maternally and Paternally Transmitted Mitochondrial Genomes of the Marine Mussel (Mytilus spp.) Genetics, June 1, 2004; 167(2): 835 - 850. [Abstract] [Full Text] [PDF]

				L. I. Grad and B. D. Lemire Mitochondrial complex I mutations in Caenorhabditis elegans produce cytochrome c oxidase deficiency, oxidative stress and vitamin-responsive lactic acidosis Hum. Mol. Genet., February 1, 2004; 13(3): 303 - 314. [Abstract] [Full Text] [PDF]

				D. R. Denver, K. Morris, and W. K. Thomas Phylogenetics in Caenorhabditis elegans: An Analysis of Divergence and Outcrossing Mol. Biol. Evol., March 1, 2003; 20(3): 393 - 400. [Abstract] [Full Text] [PDF]

				T. Ohtsuki, M. Sakurai, A. Sato, and K. Watanabe Characterization of the interaction between the nucleotide exchange factor EF-Ts from nematode mitochondria and elongation factor Tu Nucleic Acids Res., December 15, 2002; 30(24): 5444 - 5451. [Abstract] [Full Text] [PDF]

				J. L. Boore and J. L. Staton The Mitochondrial Genome of the Sipunculid Phascolopsis gouldii Supports Its Association with Annelida Rather than Mollusca Mol. Biol. Evol., February 1, 2002; 19(2): 127 - 137. [Abstract] [Full Text] [PDF]

				V. Leignel and J.-F. Humbert Mitochondrial DNA Variation in Benzimidazole-Resistant and -Susceptible Populations of the Small Ruminant Parasite Teladorsagia circumcincta J. Hered., November 1, 2001; 92(6): 503 - 506. [Abstract] [Full Text] [PDF]

				K. G. Helfenbein, W. M. Brown, and J. L. Boore The Complete Mitochondrial Genome of the Articulate Brachiopod Terebratalia transversa Mol. Biol. Evol., September 1, 2001; 18(9): 1734 - 1744. [Abstract] [Full Text] [PDF]

				D. V. Lavrov and W. M. Brown 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, February 1, 2001; 157(2): 621 - 637. [Abstract] [Full Text]

				D. R. Denver, K. Morris, M. Lynch, L. L. Vassilieva, and W. K. Thomas High Direct Estimate of the Mutation Rate in the Mitochondrial Genome of Caenorhabditis elegans Science, September 29, 2000; 289(5488): 2342 - 2344. [Abstract] [Full Text]

				Y. Noguchi, K. Endo, F. Tajima, and R. Ueshima The Mitochondrial Genome of the Brachiopod Laqueus rubellus Genetics, May 1, 2000; 155(1): 245 - 259. [Abstract] [Full Text]

				M. R. Armstrong, V. C. Blok, and M. S. Phillips A Multipartite Mitochondrial Genome in the Potato Cyst Nematode Globodera pallida Genetics, January 1, 2000; 154(1): 181 - 192. [Abstract] [Full Text]

				S.-i. Yokobori, T. Ueda, G. Feldmaier-Fuchs, S. Pääbo, R. Ueshima, A. Kondow, K. Nishikawa, and K. Watanabe Complete DNA Sequence of the Mitochondrial Genome of the Ascidian Halocynthia roretzi (Chordata, Urochordata) Genetics, December 1, 1999; 153(4): 1851 - 1862. [Abstract] [Full Text]

				K. K. A. Tetteh, A. Loukas, C. Tripp, and R. M. Maizels Identification of Abundantly Expressed Novel and Conserved Genes from the Infective Larval Stage of Toxocara canis by an Expressed Sequence Tag Strategy Infect. Immun., September 1, 1999; 67(9): 4771 - 4779. [Abstract] [Full Text] [PDF]

				C. T. Beagley, R. Okimoto, and D. R. Wolstenholme Mytilus Mitochondrial DNA Contains a Functional Gene for a tRNASer(UCN) With a Dihydrouridine Arm-Replacement Loop and a pseudo-tRNASer(UCN) Gene Genetics, June 1, 1999; 152(2): 641 - 652. [Abstract] [Full Text]

				The C. elegans Sequencing Consortium Genome Sequence of the Nematode C. elegans: A Platform for Investigating Biology Science, December 11, 1998; 282(5396): 2012 - 2018. [Abstract] [Full Text]

				J. Castresana, G. Feldmaier-Fuchs, and S. Paabo Codon reassignment and amino acid composition in hemichordate mitochondria PNAS, March 31, 1998; 95(7): 3703 - 3707. [Abstract] [Full Text] [PDF]

				S. Matsuyama, T. Ueda, P. F. Crain, J. A. McCloskey, and K. Watanabe A Novel Wobble Rule Found in Starfish Mitochondria. PRESENCE OF 7-METHYLGUANOSINE AT THE ANTICODON WOBBLE POSITION EXPANDS DECODING CAPABILITY OF tRNA J. Biol. Chem., February 6, 1998; 273(6): 3363 - 3368. [Abstract] [Full Text] [PDF]

				T. Ohtsuki, Y.-i. Watanabe, C. Takemoto, G. Kawai, T. Ueda, K. Kita, S. Kojima, Y. Kaziro, J. Nyborg, and K. Watanabe An "Elongated" Translation Elongation Factor Tu for Truncated tRNAs in Nematode Mitochondria J. Biol. Chem., June 8, 2001; 276(24): 21571 - 21577. [Abstract] [Full Text] [PDF]

				W. Y. Tsang, L. C. Sayles, L. I. Grad, D. B. Pilgrim, and B. D. Lemire Mitochondrial Respiratory Chain Deficiency in Caenorhabditis elegans Results in Developmental Arrest and Increased Life Span J. Biol. Chem., August 17, 2001; 276(34): 32240 - 32246. [Abstract] [Full Text] [PDF]

				S. J.M. Jones, D. L. Riddle, A. T. Pouzyrev, V. E. Velculescu, L. Hillier, S. R. Eddy, S. L. Stricklin, D. L. Baillie, R. Waterston, and M. A. Marra Changes in Gene Expression Associated with Developmental Arrest and Longevity in Caenorhabditis elegans Genome Res., August 1, 2001; 11(8): 1346 - 1352. [Abstract] [Full Text] [PDF]