Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-26T08:27:47.815Z Has data issue: false hasContentIssue false
  • English
  • Français

The mitochondrial genome of Angiostrongylus mackerrasae is distinct from A. cantonensis and A. malaysiensis

Published online by Cambridge University Press:  13 February 2020

Hayley Valentyne ,
David M. Spratt ,
Mahdis Aghazadeh ,
Malcolm K. Jones  and
Jan Šlapeta Open the ORCID record for Jan Šlapeta [Opens in a new window]
Hayley Valentyne
Affiliation:
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, 2006, New South Wales, Australia
David M. Spratt
Affiliation:
Australian National Wildlife Collection, National Research Collections Australia, CSIRO, GPO Box 1700, Canberra, 2601, Australia Capital Territory, Australia
Mahdis Aghazadeh
Affiliation:
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, 2006, New South Wales, Australia School of Veterinary Science, The University of Queensland, 4343, Queensland, Australia
Malcolm K. Jones
Affiliation:
School of Veterinary Science, The University of Queensland, 4343, Queensland, Australia
Jan Šlapeta*
Affiliation:
Sydney School of Veterinary Science, Faculty of Science, University of Sydney, 2006, New South Wales, Australia
*
Author for correspondence: Jan Šlapeta, E-mail: jan.slapeta@sydney.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

The native rat lungworm (Angiostrongylus mackerrasae) and the invasive rat lungworm (Angiostrongylus cantonensis) occur in eastern Australia. The species identity of A. mackerrasae remained unquestioned until relatively recently, when compilation of mtDNA data indicated that A. mackerrasae sensu Aghazadeh et al. (2015b) clusters within A. cantonensis based on their mitochondrial genomes (mtDNA). To re-evaluate the species identity of A. mackerrasae, we sought material that would be morphologically conspecific with A. mackerrasae. We combined morphological and molecular approaches to confirm or refute the specific status of A. mackerrasae. Nematodes conspecific with A. mackerrasae from Rattus fuscipes and Rattus rattus were collected in Queensland, Australia. Morphologically identified A. mackerrasae voucher specimens were characterized using amplification of cox1 followed by the generation of reference complete mtDNA. The morphologically distinct A. cantonensis, A. mackerrasae and A. malaysiensis are genetically distinguishable forming a monophyletic mtDNA lineage. We conclude that A. mackerrasae sensu Aghazadeh et al. (2015b) is a misidentified specimen of A. cantonensis. The availability of the mtDNA genome of A. mackerrasae enables its unequivocal genetic identification and differentiation from other Angiostrongylus species.

Keywords

AustraliaidentitymtDNAphylogenyspeciestaxonomy
Type
Research Article
Information
Parasitology , Volume 147 , Issue 6 , May 2020 , pp. 681 - 688
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by 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

Aghazadeh, M (2016) Molecular and pathological studies on Angiostrongylus species in southeast Queensland. In School of Veterinary Science, Vol. PhD Thesis (https://doi.org/10.14264/uql.2016.91) The University of Queensland, Australia.CrossRefGoogle Scholar
Aghazadeh, M, Reid, SA, Aland, KV, Restrepo, AC, Traub, RJ, McCarthy, JS and Jones, MK (2015a) A survey of Angiostrongylus species in definitive hosts in Queensland. International Journal for Parasitology: Parasites and Wildlife 4, 323–328.Google Scholar
Aghazadeh, M, Traub, RJ, Mohandas, N, Aland, KV, Reid, SA, McCarthy, JS and Jones, MK (2015b) The mitochondrial genome of Angiostrongylus mackerrasae as a basis for molecular, epidemiological and population genetic studies. Parasites and Vectors 8, 473.CrossRefGoogle Scholar
Aghazadeh, M, Harvie, MC, Owen, HC, Verissimo, C, Aland, KV, Reid, SA, Traub, RJ, Mc, MD, Mc, CJ and Jones, MK (2016) Comparative pathogenesis of eosinophilic meningitis caused by Angiostrongylus mackerrasae and Angiostrongylus cantonensis in murine and Guinea pig models of human infection. Parasitology 143, 1243–1251.CrossRefGoogle ScholarPubMed
Alicata, JE (1991) The discovery of Angiostrongylus cantonensis as a cause of human eosinophilic meningitis. Parasitology Today 7, 151–153.CrossRefGoogle ScholarPubMed
Barratt, J, Chan, D, Sandaradura, I, Malik, R, Spielman, D, Lee, R, Marriott, D, Harkness, J, Ellis, J and Stark, D (2016) Angiostrongylus cantonensis: a review of its distribution, molecular biology and clinical significance as a human pathogen. Parasitology 143, 1087–1118.CrossRefGoogle ScholarPubMed
Bernt, M, Donath, A, Juhling, F, Externbrink, F, Florentz, C, Fritzsch, G, Putz, J, Middendorf, M and Stadler, PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69, 313–319.CrossRefGoogle ScholarPubMed
Bhaibulaya, M (1968) A new species of Angiostrongylus in an Australian rat, Rattus fuscipes. Parasitology 58, 789–799.CrossRefGoogle Scholar
Bhaibulaya, M (1974) Experimental hybridization of Angiostrongylus mackerrasae, Bhaibulaya, 1968 and Angiostrongylus cantonensis (Chen, 1935). International Journal for Parasitology 4, 567–573.CrossRefGoogle Scholar
Bhaibulaya, M (1975) Comparative studies on the life history of Angiostrongylus mackerrasae Bhaibulaya, 1968 and Angiostrongylus cantonensis (Chen, 1935). International Journal for Parasitology 5, 7–20.CrossRefGoogle Scholar
Bhaibulaya, M (1979). Morphology and taxonomy of major Angiostrongylus species of Eastern Asia and Australia. In Cross, J (ed), Studies on Angiostrongyliasis in Eastern Asia and Australia. Taipei, Taiwan: NAMRU-2 Special Publication No. 44, pp. 4–13.Google Scholar
Bhaibulaya, M and Cross, JH (1971) Angiostrongylus malaysiensis (Nematoda: Metastrongylidae), a new species of rat lung-worm from Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 2, 527–533.Google Scholar
Blaxter, ML (2003) Nematoda: genes, genomes and the evolution of parasitism. Advances in Parasitology 54, 101–195.CrossRefGoogle ScholarPubMed
Červená, B, Modrý, D, Fecková, B, Hrazdilová, K, Foronda, P, Alonso, AM, Lee, R, Walker, J, Niebuhr, CN, Malik, R and Šlapeta, J (2019) Low diversity of Angiostrongylus cantonensis complete mitochondrial DNA sequences from Australia, Hawaii, French Polynesia and the canary islands revealed using whole genome next-generation sequencing. Parasites and Vectors 12, 241.CrossRefGoogle ScholarPubMed
Chan, D, Barratt, J, Roberts, T, Lee, R, Shea, M, Marriott, D, Harkness, J, Malik, R, Jones, M, Aghazadeh, M, Ellis, J and Stark, D (2015) The prevalence of Angiostrongylus cantonensis/mackerrasae complex in molluscs from the Sydney Region. PLoS ONE 10, e0128128.CrossRefGoogle ScholarPubMed
Chen, HT (1935) Un noveau nématode pulmonaire. Pulmonema cantonensis n.g., n.sp. des rats de Canton. Annales de Parasitologie Humaine et Comparee 13, 12–17.Google Scholar
Cowie, RH (2019) Annotated catalogue of species of Angiostrongylus and the related genera Gallegostrongylus, Rodentocaulus and Stefanskostrongylus (Nematoda: Metastrongyloidea, Angiostrongylidae). Journal of Helminthology 93, 389–423.CrossRefGoogle Scholar
Cross, JH and Bhaibulaya, M (1974) Validity of Angiostrongylus malaysiensis Bhaibulaya and Cross, 1971. Southeast Asian Journal of Tropical Medicine & Public Health 5, 374–378.Google ScholarPubMed
Dusitsittipon, S, Criscione, CD, Morand, S, Komalamisra, C and Thaenkham, U (2018) Hurdles in the evolutionary epidemiology of Angiostrongylus cantonensis: pseudogenes, incongruence between taxonomy and DNA sequence variants, and cryptic lineages. Evolutionary Applications 11, 1257–1269.CrossRefGoogle ScholarPubMed
Eamsobhana, P, Yong, HS, Song, SL, Prasartvit, A, Boonyong, S and Tungtrongchitr, A (2018) Cytochrome c oxidase subunit I haplotype reveals high genetic diversity of Angiostrongylus malaysiensis (Nematoda: Angiostrongylidae). Journal of Helminthology 92, 254–259.CrossRefGoogle Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Gasser, RB, Jabbar, A, Mohandas, N, Schnyder, M, Deplazes, P, Littlewood, DT and Jex, AR (2012) Mitochondrial genome of Angiostrongylus vasorum: comparison with congeners and implications for studying the population genetics and epidemiology of this parasite. Infection. Genetics and Evolution 12, 1884–1891.CrossRefGoogle Scholar
Hahn, C, Bachmann, L and Chevreux, B (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads – a baiting and iterative mapping approach. Nucleic Acids Research 41, e129.CrossRefGoogle ScholarPubMed
Hu, M and Gasser, RB (2006) Mitochondrial genomes of parasitic nematodes – progress and perspectives. Trends in Parasitology 22, 78–84.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lv, S, Zhang, Y, Zhang, L, Liu, Q, Liu, HX, Hu, L, Wei, FR, Steinmann, P, Graeff-Teixeira, C, Zhou, XN and Utzinger, J (2012) The complete mitochondrial genome of the rodent intra-arterial nematodes Angiostrongylus cantonensis and Angiostrongylus costaricensis. Parasitology Research 111, 115–123.CrossRefGoogle ScholarPubMed
Mackerras, MJ (1958) Catalogue of Australian mammals and their recorded internal parasites. Part II. Eutheria. Proceedings of the Linnean Society of New South Wales 83, 126–143.Google Scholar
Mackerras, MJ and Sandars, DF (1954) Life history of the rat lung-worm and its migration through the brain of its host. Nature 173, 956–957.CrossRefGoogle Scholar
Mackerras, MJ and Sandars, DF (1955) The life history of the rat lung-worm, Angiostrongylus cantonensis (Chen) (Nematoda: Metastrongylidae). Australian Journal of Zoology 3, 1–21.CrossRefGoogle Scholar
Prociv, P, Spratt, DM and Carlisle, MS (2000) Neuro-angiostrongyliasis: unresolved issues. International Journal for Parasitology 30, 1295–1303.CrossRefGoogle ScholarPubMed
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.CrossRefGoogle ScholarPubMed
Rodpai, R, Intapan, PM, Thanchomnang, T, Sanpool, O, Sadaow, L, Laymanivong, S, Aung, WP, Phosuk, I, Laummaunwai, P and Maleewong, W (2016) Angiostrongylus cantonensis and A. malaysiensis broadly overlap in Thailand, Lao PDR, Cambodia and Myanmar: a molecular survey of larvae in land snails. PLoS ONE 11, e0161128.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Hohna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Song, SL, Yong, HS and Eamsobhana, P (2018) Angiostrongylus mackerrasae and A. cantonensis (Nematoda: Metastrongyloidea) belong to same genetic lineage: evidence from mitochondrial protein-coding genes. Journal of Helminthology 92, 524–529.CrossRefGoogle Scholar
Spratt, DM (2015) Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: a review. International Journal for Parasitology: Parasites and Wildlife 4, 178–189.Google ScholarPubMed
Stockdale Walden, HD, Slapcinsky, JD, Roff, S, Mendieta Calle, J, Diaz Goodwin, Z, Stern, J, Corlett, R, Conway, J and McIntosh, A (2017) Geographic distribution of Angiostrongylus cantonensis in wild rats (Rattus rattus) and terrestrial snails in Florida, USA. PLoS ONE 12, e0177910.CrossRefGoogle ScholarPubMed
Stokes, VL, Spratt, DM, Banks, PB, Pech, RP and Williams, RL (2007) Occurrence of Angiostrongylus species (Nematoda) in populations of Rattus rattus and Rattus fuscipes in coastal forests of south-eastern Australia. Australian Journal of Zoology 55, 177–184.CrossRefGoogle Scholar
Yong, HS, Song, SL, Eamsobhana, P, Goh, SY and Lim, PE (2015a) Complete mitochondrial genome reveals genetic diversity of Angiostrongylus cantonensis (Nematoda: Angiostrongylidae). Acta Tropica 152, 157–164.CrossRefGoogle Scholar
Yong, HS, Song, SL, Eamsobhana, P, Goh, SY, Lim, PE, Chow, WL, Chan, KG and Abrahams-Sandi, E (2015b) Mitochondrial genome supports sibling species of Angiostrongylus costaricensis (Nematoda: Angiostrongylidae). PLoS ONE 10, e0134581.CrossRefGoogle Scholar
Yong, HS, Song, SL, Eamsobhana, P and Lim, PE (2016) Complete mitochondrial genome of Angiostrongylus malaysiensis Lungworm and molecular phylogeny of metastrongyloid nematodes. Acta Tropica 161, 33–40.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Valentyne et al. supplementary material

Figure S1

Download Valentyne et al. supplementary material(PDF)
PDF 258.9 KB