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Molecular characterization of two insect nematode species (Oxyurida: Thelastomatidae) using small subunit (18S) ribosomal DNA sequence and secondary-structure analyses

Published online by Cambridge University Press:  04 March 2013

A. Chaudhary ,
N. Singh  and
H.S. Singh
A. Chaudhary
Affiliation:
Molecular Taxonomy Laboratory, Department of Zoology, University Road, Chaudhary Charan Singh University, Meerut, Uttar Pradesh, India250004
N. Singh
Affiliation:
Molecular Taxonomy Laboratory, Department of Zoology, University Road, Chaudhary Charan Singh University, Meerut, Uttar Pradesh, India250004
H.S. Singh*
Affiliation:
Molecular Taxonomy Laboratory, Department of Zoology, University Road, Chaudhary Charan Singh University, Meerut, Uttar Pradesh, India250004
*
* E-mail: [email protected]
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Abstract

Nematodes of the family Thelastomatidae are parasitic in the alimentary tract of many arthropods, including Periplaneta americana L. In Meerut, Uttar Pradesh, India, two nematode species, namely Hammerschmidtiella indicus and Thelastoma icemi, belonging to this family have been reported. In the present study, the molecular phylogeny of these two nematode species was derived using small subunit (18S) sequence and secondary-structure analyses. The small subunit sequence analyses were carried out to explore the validation and systematics of these species. Phylogenetic analyses were performed for primary sequence data as well as using neighbour-joining and maximum-parsimony approaches. In contrast, the inferred secondary structures for the two species, using free-energy modelling, showed structural identities. As well as this, motif sequences were also found to be a promising tool for nematode species identification. The study provides molecular characterization based on primary sequence data of the 18S ribosomal DNA region of the nematodes along with secondary-structure data and motif sequences for inferences at higher taxonomic levels.

Type
Research Papers
Information
Journal of Helminthology , Volume 88 , Issue 2 , June 2014 , pp. 219 - 229
Copyright
Copyright © Cambridge University Press 2013 

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References

Adamson, M. (1994) Evolutionary patterns in life histories of Oxyurida. International Journal for Parasitology 24, 1167–1177.Google Scholar
Adamson, M.L. & Nasher, A.K. (1987) Hammerschmidtiella andersoni sp. n. (Thelastomatidae: Oxyurida) from the diplopod, Archispirostreptus tumuliporus in Saudi Arabia with comments on the karyotype of Hammerschmidtiella diesingi. Proceedings of the Helminthological Society of Washington 54, 220–224.Google Scholar
Adamson, M.L. & Van Waerebeke, D. (1992a) Revision of the Thelastomatoidea, Oxyurida of invertebrate hosts. 1. Thelastomatidae. Systematic Parasitology 21, 21–63.Google Scholar
Adamson, M.L. & Van Waerebeke, D. (1992b) Revision of the Thelastomatoidea, Oxyurida of invertebrate hosts. 2. Travassosinematidae, Protrelloididae and Pseudonymidae. Systematic Parasitology 21, 169–188.CrossRefGoogle Scholar
Adamson, M.L. & Van Waerebeke, D. (1992c) Revision of the Thelastomatoidea, Oxyurida of invertebrate hosts. 3. Hystrignathidae. Systematic Parasitology 22, 111–130.Google Scholar
Aleshin, V.V., Milyutina, I.A., Kedrova, O.S., Vladychenskaya, N.S. & Petrov, N.B. (1998) Phylogeny of Nematoda and Cephalorhyncha derived from 18S rDNA. Journal of Molecular Evolution 47, 597–605.Google Scholar
Anderson, R.C. (1984) The origins of zooparasitic nematodes. Canadian Journal of Zoology 62, 317–328.CrossRefGoogle Scholar
Bairoch, A. & Bucher, P. (1994) PROSITE: recent developments. Nucleic Acids Research 22, 3583–3589.Google Scholar
Basir, M.A. (1940) Nematodes parasitic in Indian cockroaches. Proceedings of Indian Academy of Sciences 12 (Sec. B), 8–16.Google Scholar
Basir, M.A. (1956) Oxyuroid parasites of Arthropoda. A monographic study. 1. Thelastomatidae 2. Oxyuridae. Zoologica (Stuttgart) 106, 1–79.Google Scholar
Bhadury, P. & Austen, M.C. (2010) Barcoding marine nematodes: an improved set of nematode 18S rRNA primers to overcome eukaryotic co-interference. Hydrobiologia 641, 245–251.Google Scholar
Biswas, P.K. & Chakravarty, G.K. (1963) The systematic studies of the zoo-parasitic oxyuroid nematodes. Zeitschrift für Parasitenkunde 23, 411–428.Google Scholar
Blanco, M.V., Lax, P., Dueñas, J.C.R., Gardenal, C.N. & Doucet, M.E. (2012) Morphological and molecular characterization of the entomoparasitic nematode Hammerschmidtiella diesingi (Nematoda Oxyurida, Thelastomatidae). Acta Parasitologica 57, 302–310.CrossRefGoogle ScholarPubMed
Chitwood, B.G. (1932) A synopsis of the nematodes parasitic in insects of the family Blattidae. Zeitschrift für Parasitenkunde 5, 14–50.CrossRefGoogle Scholar
Christie, J.R. (1931) Some nemic parasites (Oxyuridae) of coleopterous larvae. Journal of Agricultural Research 42, 463–482.Google Scholar
Cobb, N.A. (1929) The chromatropism of Mermis subnigrescens, a nemic parasite of grass-hoppers. Journal of the Washington Academy of Sciences 19, 159–166.Google Scholar
Dixon, M.T. & Hillis, D.M. (1993) Ribosomal RNA secondary structure: compensatory mutations and implications for phylogenetic analysis. Molecular Biology and Evolution 10, 256–267.Google ScholarPubMed
Duggal, C.L. & Aulakh, A. (1989) Thelastoma kherai sp. nov. and T. guptai sp. nov. (Nematoda: Thelastomatidae) from Periplaneta americana (Linnaeus) in Delhi, India. Research Bulletin (Science) of the Panjab University 40, Parts I–II, 95–98.Google Scholar
Farooqui, M.N. (1968) A new species of the genus Schwenkiella Basir, 1956 from Spirostreptus sp. Rivista di Parassitologia 29, 265–268.Google Scholar
Farooqui, M.N. (1970) Some known and new genera and species of the family Thelastomatidae Travassos, 1929. Rivista di Parassitologia 31, 195–214.Google Scholar
Fitch, D.H.A. (1997) Evolution of male tail development in rhabditid nematodes related to Caenorhabditis elegans. Systemic Biology 46, 145–179.CrossRefGoogle ScholarPubMed
Floyd, R.M., Rogers, A.D., Lambshead, P.J.D. & Smith, C.R. (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Molecular Ecology Notes 5, 611–612.Google Scholar
Gasser, R.B. (2001) Identification of parasitic nematodes and study of genetic variability using PCR approaches. pp. 53–82in Kennedy, M.W. & Harnett, W. (Eds) Parasitic nematodes: Molecular biology, biochemistry and immunology. Wallingford, CAB International.Google Scholar
Gupta, N.K. & Kaur, J. (1978) On some nematodes from invertebrates in Northern India. 1. Revista Iberica de Parasitologia 38, 301–324.Google Scholar
Hammerschmidt, K.E. (1838) Helminthologische Beitrage. Isis von Oken 5, 351–358.Google Scholar
Harris, D.J., Maia, J. & Perera, A. (2011) Molecular characterization of Hepatozoon species in reptiles from the Seychelles. Journal of Parasitology 97, 106–110.Google Scholar
Hasegawa, H., Hayashida, S., Ikeda, Y. & Sato, H. (2009) Hyper-variable regions in 18S rDNA of Strongyloides spp. as markers for species-specific diagnosis. Parasitology Research 104, 869–874.Google Scholar
Hillis, D.M. & Dixon, M.T. (1991) Ribosomal DNA molecular evolution and phylogenetic inference. The Quarterly Review of Biology 66, 410–453.Google Scholar
Honisch, M. & Krone, O. (2008) Phylogenetic relationships of Spiruromorpha from birds of prey based on 18S rDNA. Journal of Helminthology 82, 129–133.Google Scholar
Jarry, D.T. (1964) Les Oxyuroides de quelques Arthropodes dans de Midi de la France. Annales de Parasitologie Humaine et Comparée 39, 381–508.Google Scholar
Jarry, D.M. & Jarry, D.T. (1968) Tentative de classification à propos de 60 espèces des genres Cephalobellus et Thelastoma (Nematoda- Oxyuroidea) (Attempt at clarifying 60 species of Cephalobellus and Thelastoma family (Nematoda-Oxyuroidea)). Annales de Parasitologie Humaine et Comparée 43, 339–352.CrossRefGoogle ScholarPubMed
Jex, A.R., Schneider, M.A., Rose, H.A. & Cribb, T.H. (2005) The Thelastomatoidea (Nematoda: Oxyurida) of two sympatric Panesthiinae (Insecta: Blattodea) from south-eastern Queensland, Australia: taxonomy, species richness and host specificity. Nematology 7, 543–575.Google Scholar
Jex, A.R., Hu, M., Rose, H.A., Schneider, M., Cribb, T.H. & Gasser, R.B. (2006) Molecular characterization of Thelastomatoidea (Nematoda: Oxyurida) from cockroaches in Australia. Parasitology 133, 123–129.Google Scholar
Jones, R., Brown, D.S., Harris, E., Jones, J., Symondson, W.O.C., Bruford, M.W. & Cable, J. (2012) First record of Neoxysomatium brevicaudatum through the non-invasive sampling of Anguis fragilis: complementary morphological and molecular detection. Journal of Helminthology 86, 125–129.CrossRefGoogle ScholarPubMed
Keller, A., Forster, F., Müller, T., Dandekar, T., Schultz, J. & Wolf, M. (2010) Including RNA secondary structures improves accuracy and robustness in reconstruction of phylogenetic trees. Biology Direct 5, 4.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.Google Scholar
Kloss, G.R. (1965) Considerases em toruo de Thelastoma Leidy, 1850 Cephalobellus Cobb, 1920 (Nematoda). Papéis Avulsos de Zoologia (São Paulo) 17, 131–179.Google Scholar
Leibersperger, E. (1960) Die Oxyuroidea der europäischen Arthropoden. Parasitologische Schiftenreihe 11, 1–149.Google Scholar
Leidy, J. (1849) New genera and species of Entozoa. Proceedings of the National Academy of Sciences of the United States of America 4, 225–233.Google Scholar
Leidy, J. (1851) Contribution to helminthology. Proceedings of the National Academy of Sciences, Philadelphia 5, 205–209.Google Scholar
Ma, H., Overstreeta, R.M. & Subbotin, S.A. (2008) ITS2 secondary structure and phylogeny of cyst-forming nematodes of the genus Heterodera (Tylenchida: Heteroderidae). Organisms, Diversity and Evolution 8, 182–193.Google Scholar
Maia, J.P.M.C., Harris, D.J. & Perera, A. (2011) Molecular survey of Hepatozoon species in lizards from North Africa. Journal of Parasitology 97, 513–517.Google Scholar
Olsen, G.J. & Woese, C.R. (1993) Ribosomal RNA – a key to phylogeny. FASEB Journal 7, 113–123.Google Scholar
Parveen, R. & Jairajpuri, D.S. (1980) A new species of the genus Schwenkiella Basir, 1956 from cockroach, Periplaneta americana, from Aligarh. Indian Journal of Parasitology 4, 41–43.Google Scholar
Parveen, R. & Jairajpuri, D.S. (1981) Two new species of insect nematodes of the family Thelastomatidae. Rivista di Parassitologia 42, 261–266.Google Scholar
Parveen, R. & Jairajpuri, D.S. (1983) Schwenkiella atheri sp. nov. (Nematode: Thelastomatidae) a new nematode parasite of the common cockroach, Periplaneta americana. Indian Journal of Nematology 13, 209–212.Google Scholar
Perera, A., Maia, J.P.M.C., Jorge, F. & Harris, D.J. (2012) Molecular screening of nematodes in lacertid lizards from the Iberian Peninsula and Balearic Islands using 18S rRNA sequences. Journal of Helminthology. Published online 2 April 2012, doi:10.1017/S0022149X12000181Google Scholar
Rao, P.N. (1958) Studies on the nematode parasites of insects and other arthropods. Arquivos do Museu Nacional 46, 33–83.Google Scholar
Rao, P.N. & Rao, V.J. (1965) A description of a new species of the genus Hammerschmidtiella Chitwood, 1932 (Nematoda: Oxyuridae). Rivista di Parassitologia 26, 9–12.Google Scholar
Rizvi, A.N. & Jairajpuri, D.S. (1995) Scanning electron microscopy of Thelastoma atheri n. comb. (Nematoda: Thelastomatidae), from the cockroach, Periplaneta americana. Journal of Parasitology and Applied Animal Biology 4, 9–13.Google Scholar
Ross, J.L., Ivanova, E.S., Spiridonov, S.E., Waeyenberge, L., Moens, M., Nicol, G.W. & Wilson, M.J. (2010) Molecular phylogeny of slug-parasitic nematodes inferred from 18S rRNA gene sequences. Molecular Phylogenetics and Evolution 55, 738–743.Google Scholar
Schultz, J., Maisel, S., Gerlach, D., Müller, T. & Wolf, M. (2005) A common core of secondary structure of the internal transcribed spacer 2 (ITS2) throughout the Eukaryota. RNA 11, 361–364.Google Scholar
Schwenk, J.M. (1926) Fauna parasitologia des blattoides do Brasil. Sciencia Medica; Anno, IV 9, 3–16.Google Scholar
Shah, M.M. (2007) Some studies on insect parasitic nematodes (Oxyurida, Thelastomatoidea, Thelastomatidae) from Manipur, North-East India. Acta Parasitologica 52, 346–362.Google Scholar
Sharma, R.K. & Gupta, L.N. (1983) A new entomogenous nematode, Hammerschmidtiella bareillyi from Periplaneta americana. Revista Iberica de Parasitologia 43, 319–323.Google Scholar
Siebert, S. & Backofen, R. (2005) MARNA: multiple alignment and consensus structure prediction of RNAs based on sequence structure comparisons. Bioinformatics 21, 3352–3359.Google Scholar
Singh, H.S. & Kaur, H. (1988) On a new nematode, Hammerschmidtiella bisiri n. sp. from Periplaneta americana Linn. Indian Journal of Parasitology 12, 187–189.Google Scholar
Singh, H.S. & Malti, (2003) Studies of some nematode parasites of Periplanata americana Linn. at Meerut, Uttar Pradesh, India. Flora and Fauna 2, 59–66.Google Scholar
Singh, K.S. (1955) Two species of nematodes from a millipede from India. Revista Ibérica Parasitología (Libra Hom Prof. Lopee Neyra) 35–44.Google Scholar
Singh, K.S. & Singh, K.P. (1955) On some nematodes from invertebrates. Records of the Indian Museum 53, 37–51.Google Scholar
Skrjabin, K.I., Shikobalova, N.P. & Mozgovoj, A.A. (1951) Opredelitel' paraziticheskikh nematod. Vol. 2. Oxyurata i Askaridata. Moscow, Nauka (in Russian).Google Scholar
Skrjabin, K.I., Shikobalova, N.P., Sobolev, A.A., Paramonov, A.A. & Sudarikov, V.E. (1954) Opredelitel' paraziticheskikh nematod, Tom IV. Camallanata, Rhabdidata, Tilenchata, Trichocephalata, Dioctofimata, i razpredelenie paraziticheskikh nematod pokhozyaevam. Moscow, Nauka (in Russian).Google Scholar
Skrjabin, K.I., Shikobalova, N.P. & Lagodovskaya, E.A. (1966) Oxyuraty chlenistonogikh Part 4. Osnovy nematodologii. Moscow, Nauka (in Russian).Google Scholar
Subbotin, S.A., Sturhan, D., Vovlas, N., Castillo, P., Tambe, J.T., Moens, M. & Baldwin, J.G. (2007) Application of the secondary structure model of rRNA for phylogeny: D2–D3 expansion segments of the LSU gene of plant-parasitic nematodes from the family Hoplolaimidae Filipjev, 1934. Molecular Phylogenetics and Evolution 43, 881–890.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Travassos, L. (1929) Contribuicno preliminary a sistemática dos nematodeos dos artropodes. Memorias do Instituto Oswaldo Cruz 5, 19–25.Google Scholar
Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31, 3406–3415.Google Scholar
Zwieb, C., Glotz, C. & Brimacombe, R. (1981) Secondary structure comparisons between small subunit ribosomal RNA molecules from six different species. Nucleic Acids Research 9, 3621–3640.Google Scholar