Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-26T12:16:42.629Z Has data issue: false hasContentIssue false

Phylogenetics and systematics of Angiostrongylus lungworms and related taxa (Nematoda: Metastrongyloidea) inferred from the nuclear small subunit (SSU) ribosomal DNA sequences

Published online by Cambridge University Press:  13 March 2014

P. Eamsobhana*
Affiliation:
Department of Parasitology, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok10700, Thailand
P.E. Lim
Affiliation:
Institute of Biological Sciences, University of Malaya, 50603Kuala Lumpur, Malaysia Institute of Ocean and Earth Sciences, University of Malaya, 50603Kuala Lumpur, Malaysia
H.S. Yong
Affiliation:
Institute of Biological Sciences, University of Malaya, 50603Kuala Lumpur, Malaysia

Abstract

The Angiostrongylus lungworms are of public health and veterinary concern in many countries. At the family level, the Angiostrongylus lungworms have been included in the family Angiostrongylidae or the family Metastrongylidae. The present study was undertaken to determine the usefulness and suitability of the nuclear 18S (small subunit, SSU) rDNA sequences for differentiating various taxa of the genus Angiostrongylus, as well as to determine the systematics and phylogenetic relationship of Angiostrongylus species and other metastrongyloid taxa. This study revealed six 18S (SSU) haplotypes in A. cantonensis, indicating considerable genetic diversity. The uncorrected pairwise ‘p’ distances among A. cantonensis ranged from 0 to 0.86%. The 18S (SSU) rDNA sequences unequivocally distinguished the five Angiostrongylus species, confirmed the close relationship of A. cantonensis and A. malaysiensis and that of A. costaricensis and A. dujardini, and were consistent with the family status of Angiostrongylidae and Metastrongylidae. In all cases, the congeneric metastrongyloid species clustered together. There was no supporting evidence to include the genus Skrjabingylus as a member of Metastrongylidae. The genera Aelurostrongylus and Didelphostrongylus were not recovered with Angiostrongylus, indicating polyphyly of the Angiostrongylidae. Of the currently recognized families of Metastrongyloidea, only Crenosomatidae appeared to be monophyletic. In view of the unsettled questions regarding the phylogenetic relationships of various taxa of the metastrongyloid worms, further analyses using more markers and more taxa are warranted.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2014 

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

Anderson, R.C. (2000) Nematode parasites of vertebrates: Their development and transmission. 2nd edn. 650 pp. Wallingford, UK, CABI Publishing/CAB International.Google Scholar
Bhadury, P., Austen, M.C., Bilton, D.T., Lambshead, P.J.D., Rogers, A.D. & Smerdon, G.R. (2006) Development and evaluation of a DNA-barcoding approach for the rapid identification of nematodes. Marine Ecology Progress Series 320, 19.Google Scholar
Bhaibulaya, M. & Cross, J.H. (1971) Angiostrongylus malaysiensis (Nematoda: Metastrongylidae), a new species of rat lungworm from Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 2, 527533.Google Scholar
Blaxter, M.L., De Ley, P., Garey, J.R., Liu, L.X., Scheldeman, P., Vierstraete, A., Vanfleteren, J.R., Mackey, L.Y., Dorris, M., Frisse, L.M., Vida, J.T. & Thomas, W.K. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175.Google Scholar
Caldeira, R.L., Carvalho, O.S., Mendonca, C.L.F.G., Graeff-Teixeira, C., Silva, M.C.F., Ben, R., Maurer, R., Lima, W.S. & Lenzi, H.L. (2003) Molecular differentiation of Angiostrongylus costaricensis, A. cantonensis and A. vasorum by polymerase chain reaction-restriction fragment length polymorphism. Memórias do Instituto Oswaldo Cruz 108, 116118.Google Scholar
Carreno, R.A. & Nadler, S.A. (2003) Phylogenetic analysis of the Metastrongyloidea (Nematoda: Strongylidae) inferred from ribosomal RNA gene sequences. Journal of Parasitology 89, 965973.Google Scholar
Carreno, R.A., Reif, K.E. & Nadler, S.A. (2005) A new species of Skrjabingylus Petrov, 1927 (Nematoda: Metastrongyloidea) from the frontal sinuses of the hooded skunk, Mephitis macroura (Mustelidae). Journal of Parasitology 91, 102107.Google Scholar
Conboy, G.A. (2011) Canine angiostrongylosis: the French heartworm: an emerging threat in North America. Veterinary Parasitology 176, 382389.Google Scholar
Cross, J.H. (1979) Experimental studies on Angiostrongylus species in monkeys and laboratory animals. pp. 118137 in Cross, J.H. (Ed.) Studies on angiostrongyliasis in Eastern Asia and Australia. Taipei, Taiwan, . US Naval Medical Research Unit No. 2.Google Scholar
Cross, J.H. & Chen, E.R. (2007) Angiostrongyliasis. pp. 263290 in Murrel, K.D. & Fried, B. (Eds) Food borne parasitic zoonoses. New York, Springer.Google Scholar
Eamsobhana, P. (2006) The rat lungworm Parastrongylus (= Angiostrongylus) cantonensis: Parasitology, immunology, eosinophilic meningitis, epidemiology and laboratory diagnosis. 156 pp. Bangkok, Wankaew (IQ), Book Center Co. Ltd.Google Scholar
Eamsobhana, P. & Tungtrongchitr, A. (2005) Angiostrongyliasis in Thailand. pp. 3247 in Arizono, N., Chai, J.Y., Nawa, Y. & Takahashi, T. (Eds) Food-borne helminthiasis in Asia. Chiba, Japan, The Federation of Asian Parasitologists.Google Scholar
Eamsobhana, P. & Yong, H.S. (2009) Immunological diagnosis of human angiostrongyliasis due to Angiostrongylus cantonensis (Nematoda: Angiostrongylidae). International Journal of Infectious Diseases 13, 425431.Google Scholar
Eamsobhana, P., Lim, P.E., Zhang, H., Gan, X. & Yong, H.S. (2010a) Molecular differentiation and phylogenetic relationships of three Angiostrongylus species and Angiostrongylus cantonensis geographical isolates based on a 66-kDa protein gene of A. cantonensis (Nematoda: Angiostrongylidae). Experimental Parasitology 126, 564569.Google Scholar
Eamsobhana, P., Lim, P.E., Solano, G., Zhang, H., Gan, X. & Yong, H.S. (2010b) Molecular differentiation of Angiostrongylus taxa (Nematoda: Angiostrongylidae) by cytochrome c oxidase subunit I (COI) gene sequences. Acta Tropica 116, 152156.Google Scholar
Eamsobhana, P., Lim, P.E. & Yong, H.S. (2013) Molecular phylogeny of filarial worms (Nematoda: Filarioidea). The Raffles Bulletin of Zoology Supplement 29, 99109.Google Scholar
Fontanilla, I.K.C. & Wade, C.M. (2008) The small subunit (SSU) ribosomal (r) RNA as a genetic marker for identifying infective 3rd juvenile stage Angiostrongylus cantonensis . Acta Tropica 105, 181186.Google Scholar
Foronda, P., López-González, M., Miquel, J., Torres, J., Segovia, M., Abreu-Acosta, N., Casanova, J.C., Valladares, B., Mas-Coma, S., Bargues, M.D. & Feliu, C. (2010) Finding of Parastrongylus cantonensis (Chen, 1935) in Rattus rattus in Tenerife, Canary Islands (Spain). Acta Tropica 114, 123127.Google Scholar
Gasser, R.B. & Newton, S.E. (2000) Genomic and genetic research on bursate nematodes: significance, implications and prospects. International Journal of Parasitology 30, 509534.Google Scholar
Graeff-Teixeira, C. (2010) Current status of the diagnosis of abdominal angiostrongyliasis. pp. 4145 in Eamsobhna, P. (Ed.) Angiostrongylus and angiostrongyliasis – Advances in the disease, control, diagnosis and molecular genetics. Bangkok, Thailand, Mahidol University.Google Scholar
Graeff-Teixeira, C., da Silva, A.C.A. & Yoshimura, K. (2009) Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Review 22, 322348.Google Scholar
Hall, T.A. (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Holterman, M., van der Wulff, , van den Elsen, S., van Megan, H., Bongers, T., Holovachov, O., Bakker, J. & Helder, J. (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23, 17921800.Google Scholar
Jefferies, R., Shaw, S.E., Viney, M.E. & Morgan, E.R. (2009) Angiostrongylus vasorum from South America and Europe represent distinct lineages. Parasitology 136, 107115.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Jounal of Molecular Evolution 16, 111120.Google Scholar
Kliks, M.M. & Palumbo, N.E. (1992) Eosinophilic meningitis beyond the Pacific Basin: the global dispersal of a peridomestic zoonosis caused by Angiostrongylus cantonensis, the nematode lungworm of rats. Social Science and Medicine 34, 199212.Google Scholar
Maldonado, A. Jr, Simŏes, R. & Thiengo, S. (2012) Angiostrongyliasis in the Americas. pp. 303320 in Lorenzo-Morales, J. (Ed.) Zoonosis. InTech, available at www.intechopen.com (accessed accessed 4 December 2012).Google Scholar
Morgan, E.R., Shaw, S.E., Brennan, S.F., De Waal, T.D., Jones, B.R. & Mulcahy, G. (2005) Angiostrongylus vasorum: a real heartbreaker. Trends in Parasitology 21, 4951.Google Scholar
Myers, P., Espinosa, R., Parr, C.S., Jones, T., Hammond, G.S. & Dewey, T.A. (2013) The animal diversity web Available at http://animaldiversity.org (accessed accessed 26 June 2013).Google Scholar
Smythe, A.B., Sanderson, M.J. & Nadler, S.A. (2006) Nematode small subunit phylogeny correlates with alignment parameters. Systematic Biology 55, 972992.Google Scholar
Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.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, 27312739.Google Scholar
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.Google Scholar
Tokiwa, T., Harunari, T., Tanikawa, T., Komatsu, N., Koizumi, N., Tung, K.-C., Suzuki, J., Kadasaka, T., Takada, N., Kumagai, T., Akao, N. & Ohta, N. (2012) Phylogenetic relationships of rat lungworm, Angiostrongylus cantonensis, isolated from different geographical regions revealed widespread multiple lineages. Parasitology International 61, 431436.Google Scholar
Van Megan, H., van den Elsen, S., Holerman, M., Karssen, G., Mooyman, P., Bongers, T., Holovachov, O., Bakker, J. & Helder, J. (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11, 927950.Google Scholar