Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-25T14:02:18.396Z Has data issue: false hasContentIssue false
  • English
  • Français

Mitochondrial DNA dataset suggest that the genus Sphaerirostris Golvan, 1956 is a synonym of the genus Centrorhynchus Lühe, 1911

Published online by Cambridge University Press:  03 June 2020

Nehaz Muhammad ,
Suleman ,
Munawar Saleem Ahmad ,
Liang Li ,
Qing Zhao ,
Hanif Ullah Open the ORCID record for Hanif Ullah [Opens in a new window] ,
Xing-Quan Zhu  and
Jun Ma Open the ORCID record for Jun Ma [Opens in a new window]
Nehaz Muhammad
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province730046, P.R. China
Suleman
Affiliation:
Department of Zoology, University of Swabi, Swabi, Khyber Pakhtunkhwa, Pakistan
Munawar Saleem Ahmad
Affiliation:
Department of Zoology, University of Swabi, Swabi, Khyber Pakhtunkhwa, Pakistan
Liang Li*
Affiliation:
Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, 050024Shijiazhuang, Hebei Province, P.R. China
Qing Zhao
Affiliation:
Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, 050024Shijiazhuang, Hebei Province, P.R. China
Hanif Ullah
Affiliation:
Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Key Laboratory of Animal Parasitology, Shanghai20041, PR China
Xing-Quan Zhu
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province730046, P.R. China Jiangsu Co-innovation Centre for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University College of Veterinary Medicine, Yangzhou, Jiangsu Province225009, PR China
Jun Ma
Affiliation:
State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu Province730046, P.R. China
*
Author for correspondence: Liang Li, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Our present genetic data of Acanthocephala, especially the mitochondrial (mt) genomes, remains very limited. In the present study, the nearly complete mt genome sequences of Sphaerirostris lanceoides (Petrochenko, 1949) was sequenced and determined for the first time based on specimens collected from the Indian pond heron Ardeola grayii (Sykes) (Ciconiiformes: Ardeidae) in Pakistan. The mt genome of S. lanceoides is 13 478 bp in size and contains 36 genes, including 12 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs) and two ribosomal RNA genes (rRNAs). Moreover, in order to clarify the phylogenetic relationship of the genera Centrorhynchus and Sphaerirostris, and to test the systematic position of S. lanceoides in the Centrorhynchidae, the phylogenetic analyses were performed using Bayesian inference and maximum likelihood methods, based on concatenated nucleotide sequences of 12 PCGs, rRNAs and tRNAs. The phylogenetic results further confirmed the monophyly of the order Polymorphida and the paraphyly of the order Echinorhynchida in the class Palaeacanthocephala. Our results also challenged the validity of the genus Sphaerirostris (Polymorphida: Centrorhynchidae) and showed a sister relationship between S. lanceoides and S. picae (Rudolphi, 1819).

Keywords

AcanthocephalaCentrorhynchidaemitochondrial genomephylogenySphaerirostrissystematics
Type
Research Article
Information
Parasitology , Volume 147 , Issue 10 , September 2020 , pp. 1149 - 1157
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

Amin, OM (2013) Classification of the Acanthocephala. Folia Parasitologica 60, 273–305.CrossRefGoogle ScholarPubMed
Amin, OM and Canaris, A (1997) Description of Neolacunisoma Geraldschmidti gen. n., sp. n., (Acanthocephala: Centrorhynchidae) from South African shorebirds. Journal of Helminthological Society of Washington 64, 275–280.Google Scholar
Amin, OM and Ha, NV (2008) On a new acanthocephalan family and a new order, from birds in Vietnam. Journal of Parasitology 94, 1305–1310.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Halajian, A and Eslami, A (2010) Redescription of Sphaerirostris Picae (Acanthocephala: Centrorhynchidae) from magpie, Pica pica, in northern Iran, with special reference to unusual receptacle structures and notes on histopathology. Journal of Parasitology 96, 561–568.CrossRefGoogle ScholarPubMed
Bernt, M, Donath, A, Juhling, F, Externbrink, F, Florentz, C, Fritzsch, G, Putz, M, Middendorf, M and Stadler, PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69, 313–319.CrossRefGoogle ScholarPubMed
Burland, (2000) DNASTAR's Lasergene sequence analysis software. Methods Molecular Biology 132, 71–91.Google ScholarPubMed
Dimitrova, ZM, Murai, E and Genov, T (1995) Some species of the family Centrorhynchidae Van Cleave, 1916 (Acanthocephala) from Hungarian birds. Parasitologia Hungarica 28, 89–99.Google Scholar
Dimitrova, ZM, Georgiev, BB and Genov, T (1997) Acanthocephalans of the family Centrorhynchidae (Palaeacanthocephala) from Bulgaria. Folia Parasitologica 44, 224–232.Google Scholar
García-Varela, M and González-Oliver, A (2008) The systematic position of Leptorhynchoides (Kostylew, 1924) and Pseudoleptorhynchoides (Salgado-Maldonado, 1976), inferred from nuclear and mitochondrial DNA gene sequences. Journal of Parasitology 94, 959–962.CrossRefGoogle Scholar
García-Varela, M and Nadler, SA (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. Journal of Parasitology 91, 1401–1409.CrossRefGoogle ScholarPubMed
García-Varela, M and Nadler, SA (2006) Phylogenetic relationships among Syndermata inferred from nuclear and mitochondrial gene sequences. Molecular Phylogenetics and Evolution 40, 61–72.CrossRefGoogle ScholarPubMed
García-Varela, M, Perez-Ponce de Leon, G, De la Torre, P, Cummings, MP, Sarma, SS and Laclette, JP (2000) Phylogenetic relationships of Acanthocephala based on analysis of 18S ribosomal RNA gene sequences. Journal of Molecular Evolution 50, 532–540.CrossRefGoogle ScholarPubMed
García-Varela, M, Cummings, MP, Perez-Ponce de Leon, G, Gardner, SL and Laclette, JP (2002) Phylogenetic analysis based on 18S ribosomal RNA gene sequences supports the existence of class Polyacanthocephala (Acanthocephala). Molecular Phylogenetics and Evolution 23, 288–292.CrossRefGoogle Scholar
Gasser, RB, Hu, M, Chilton, NB, Campbell, BE, Jex, AJ, Otranto, D, Cafarchia, C, Beveridge, I and Zhu, XQ (2006) Single strand conformation polymorphism (SSCP) for the analysis of genetic variation. Nature Protocols 1, 3121–3128.CrossRefGoogle ScholarPubMed
Gazi, M, Sultana, T, Min, GS, Park, YC, García-Varela, M, Nadler, SA and Park, JK (2012) The complete mitochondrial genome sequence of Oncicola Luehei (Acanthocephala: Archiacanthocephala) and its phylogenetic position within Syndermata. Parasitology International 61, 307–316.CrossRefGoogle ScholarPubMed
Gazi, M, Kim, J and Park, JK (2015) The complete mitochondrial genome sequence of Southwellina hispida supports monophyly of Palaeacanthocephala (Acanthocephala: Polymorphida). Parasitology International 6, 64–68.CrossRefGoogle Scholar
Gazi, M, Kim, J, García-Varela, M, Park, C, Littlewood, DTJ and Park, JK (2016) Mitogenomic phylogeny of Acanthocephala reveals novel Class relationships. Zoological Scripta 45, 437–454.CrossRefGoogle Scholar
Golvan, YJ (1956) Le genre Centrorhynchus Lühe 1911 (Acanthocephala-Polymorphidae). Révision des espèces européennes et description dune nouvelle espèce africaine parasite de rapace diurne. Bulletin de l'Institut Fondamental d'Afrique Noire (Ser. A) 18, 732–785.Google Scholar
Golvan, YJ (1969) Systematique des acanthocephales (Acanthocephala Rudolphi 1801). Premiere partie. L'ordre des Palaeacanthocephala Meyer 1931. Premier fascicule. La super-famille des Echinorhynchoidea (Cobbold 1876) Golvan et Houin 1963. Memoires du Museum National d'Histoire Naturelle, Nouvelle Serie, Serie A, Zoologie 57, 1–373.Google Scholar
Kalyaanamoorthy, S, Minh, BQ, Wong, TKF, Von Haeseler, A and Jermiin, LS (2017) Modelfinder: fast model selection for accurate phylogenetic estimates. Nature Methods 6, 587–589.CrossRefGoogle Scholar
Kang, J and Li, L (2018) First report on cystacanths of Sphaerirostris lanceoides (Petrochenko, 1949) (Acanthocephala: Centrorhynchidae) from the Asiatic toad Bufo gargarizans Cantor (Amphibia: Anura) in China. Systematics Parasitology 95, 447–454.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Laslett, D and Canback, B (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics (Oxford, England) 24, 172–175.CrossRefGoogle ScholarPubMed
Letunic, I and Bork, P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Research 44, 242–245.CrossRefGoogle ScholarPubMed
Lisitsyna, OI, Kudlai, O, Cribb, TH and Smit, NJ (2019) Three new species of acanthocephalans (Palaeacanthocephala) from marine fishes collected off the East Coast of South Africa. Folia Parasitol (Praha) 6, 012.Google Scholar
Minh, BQ, Nguyen, MAT and Von Haeseler, A (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30, 1188–1195.CrossRefGoogle ScholarPubMed
Muhammad, N, Ma, J, Khan, MS, Li, L, Zhao, Q, Ahmad, MS and Zhu, XQ (2019a) Characterization of the complete mitochondrial genome of Sphaerirostris picae (Rudolphi, 1819) (Acanthocephala: Centrorhynchidae), representative of the genus Sphaerirostris. Parasitology Research 118, 2213–2221.CrossRefGoogle Scholar
Muhammad, N, Ma, J, Khan, MS, Wu, SS, Zhu, XQ and Li, L (2019b) Characterization of the complete mitochondrial genome of Centrorhynchus Milvus (Acanthocephala: Polymorphida) and its phylogenetic implications. Infection, Genetics, and Evolution 75, 103946.CrossRefGoogle Scholar
Muhammad, N, Khan, MS, Li, L, Zhao, Q, Ullah, H, Zhu, XQ and Ma, J (2020a) Characterization of the complete mitogenome of Centrorhynchus clitorideus (Meyer, 1931) (Palaeacanthocephala: Centrorhynchidae), the largest mitochondrial genome in Acanthocephala, and its phylogenetic implications. Molecular and Biochemical Parasitology 237, 111274.CrossRefGoogle Scholar
Muhammad, N, Li, L, Zhao, Q, Bannai, MA, Mohammad, ET, Khan, MS and Ma, J (2020b) Characterization of the complete mitochondrial genome of Cavisoma magnum (Acanthocephala: Palaeacanthocephala), first representative of the family Cavisomidae, and its phylogenetic implications. Infection, Genetics, and Evolution 80, 104173.CrossRefGoogle Scholar
Near, TJ (2002) Acanthocephalan phylogeny and the evolution of parasitism. Integrative Comparative Biology 42, 668–677.CrossRefGoogle ScholarPubMed
Near, TJ, Garey, JR and Nadler, SA (1998) Phylogenetic relationships of the Acanthocephala inferred from 18S ribosomal DNA sequences. Molecular Phylogenetics and Evolution 10, 287–298.CrossRefGoogle ScholarPubMed
Nguyen, LT, Schmidt, HA, Von Haeseler, A and Minh, BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.CrossRefGoogle ScholarPubMed
Pan, T and Jiang, H (2018) The complete mitochondrial genome of Hebesoma Violentum (Acanthocephala). Mitochondrial DNA Part B 3, 582–583.CrossRefGoogle Scholar
Pan, TS and Nie, P (2013) The complete mitochondrial genome of Pallisentis celatus (Acanthocephala) with phylogenetic analysis of acanthocephalans and rotifers. Folia Parasitologica 60, 181–191.CrossRefGoogle ScholarPubMed
Pichelin, S and Cribb, TH (2001) The status of the Diplosentidae (Acanthocephala: Palaeacanthocephala) and a new family of acanthocephalans from Australian wrasses (Pisces: Labridae). Folia Parasitologica 48, 289–303.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Van der Mark, P, Ayres, DL, Darling, A, Höhna, 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
Sato, H, Suzuki, K, Uni, S and Kamiya, H (2005) Recovery of the everted cystacanth of seven acanthocephalan species of birds from feral raccoons (Procyon lotor) in Japan. Journal of Veterinary Medical Science 67, 1203–1206.CrossRefGoogle ScholarPubMed
Sato, H, Suzuki, K and Aoki, M (2006) Juvenile bird acanthocephalans recovered incidentally from raccoon dogs Nyctereutes procyonoides viverrinus on Yakushima Island, Japan. Journal of Veterinary Medical Science 68, 689–692.CrossRefGoogle ScholarPubMed
Song, R, Zhang, D, Deng, S, Ding, D, Liao, F and Liu, L (2016) The complete mitochondrial genome of Acanthosentis Cheni (Acanthocephala: Quadrigyridae). Mitochondrial DNA Part B Resources 1, 797–798.CrossRefGoogle Scholar
Song, R, Zhang, D, Gao, JW, Cheng, XF, Xie, M, Li, H and Wu, YA (2019) Characterization of the complete mitochondrial genome of Brentisentis yangtzensis Yu and Wu, 1989 (Acanthocephala, Illiosentidae). Zoo Keys 861, 1–14.Google Scholar
Steinauer, ML, Nickol, BB, Broughton, R and Ortí, G (2005) First sequenced mitochondrial genome from the phylum Acanthocephala (Leptorhynchoides Thecatus) and its phylogenetic position within Metazoa. Journal of Molecular Evolution 60, 706–715.CrossRefGoogle ScholarPubMed
Talavera, G and Castresana, J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.CrossRefGoogle ScholarPubMed
Torracca, B, Macchioni, F, Masetti, M, Gabrielli, S, Guardone, L, Prati, MC and Magi, M (2010) First recovery of bird acanthocephalan Sphaerirostris lanceoides In an Eurasian badger (Meles meles) in Italy. Hystrix the Italian Journal of Mammalogy 21, 195–198.Google Scholar
Verweyen, L, Klimpel, S and Palm, HW (2011) Molecular phylogeny of the Acanthocephala (class Palaeacanthocephala) with a paraphyletic assemblage of the orders Polymorphida and Echinorhynchida. PloS One 6, e28285.CrossRefGoogle ScholarPubMed
Weber, M, Wey-Fabrizius, AR, Podsiadlowski, L, Witek, A, Schill, RO, Sugár, L and Hankeln, T (2013) Phylogenetic analyses of endoparasitic Acanthocephala based on mitochondrial genomes suggest secondary loss of sensory organs. Molecular Phylogenetics and Evolution 66, 182–189.CrossRefGoogle ScholarPubMed
Wickham, (2016) ggplot2: Elegant Graphics for Data Analysis. NewYork: Springer-Verlag.CrossRefGoogle Scholar
Zhang, D, Gao, F, Jakovlić, I, Zou, H, Zhang, J, Li, WX and Wang, GT (2020) Phylosuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20, 348–355.CrossRefGoogle ScholarPubMed