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A new species of Hepatozoon Miller, 1908 (Apicomplexa: Adelerina) from the snake Philodryas nattereri Steindachner (Squamata: Dipsadidae) in northeastern Brazil

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Abstract

Based on both unique morphological characteristics of the gamont, distinct changes caused to the host erythrocyte and analysis of partial 18S rRNA gene sequences, a new parasite of the genus Hepatozoon Miller, 1908 is described from the snake Philodryas nattereri Steindachner (Squamata: Dipsadidae) in northeastern Brazil. The new species, Hepatozoon musa n. sp., is characterized by large and curved mature gamonts (18.9 ± 0.9 μm in length and 3.8 ± 0.3 μm in width) that considerably engorge infected host erythrocytes and displace the nucleus laterally, which become longer and thinner. Phylogenetic estimates indicate the new species is more closely related to the recently described Hepatozoon cuestensis O’Dwyer, Moço, Paduan, Spenassatto, Silva & Ribolla, 2013, from Brazilian rattlesnakes. These recent findings highlight the need for further studies of Hepatozoon to better determine the biodiversity of this common but poorly-studied parasite group.

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References

  • Abramoff, M. D., Magalhães, P. J., & Ram, S. J. (2004). Image processing with ImageJ. Biophotonics International, 11, 36–42.

    Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Barta, J. R., Ogedengbe, J. D., Martin, D. S., & Smith, T. G. (2012). Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rDNA sequences. Journal of Eukaryotic Microbiology, 59, 171–180.

    Article  CAS  PubMed  Google Scholar 

  • Carini, A. (1910). Sobre uma hemogregarina de Philodryas schottii. Revista de Medicina (São Paulo), 23, 339–340.

    Google Scholar 

  • França, F. G. R., Mesquita, D. O., Nogueira, C. C., & Araújo, A. F. B. (2008). Phylogeny and Ecology Determine Morphological Structure in a Snake Assemblage in the Central Brazilian Cerrado. Copeia, 1, 23–28.

    Article  Google Scholar 

  • Freitas, M. A. (2014). Squamate reptiles of the Atlantic Forest of northern Bahia, Brazil. Check List, 10, 1020–1030.

    Article  Google Scholar 

  • Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate Maximum-Likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.

    Article  CAS  PubMed  Google Scholar 

  • Haklová-Kočíková, B., Hižňanová, A., Majláth, I., Račka, K., Harris, D. J., Földvári, G., et al. (2014). Morphological and molecular characterization of Karyolysus - a neglected but common parasite infecting some European lizards. Parasites & Vectors, 7, 555.

    Google Scholar 

  • Hamdan, B., & Lira-da-Silva, R. M. (2012). The snakes of Bahia State, northeastern Brazil: species richness, composition and biogeographical notes. Salamandra, 48, 31–50.

    Google Scholar 

  • Harris, D. J., Borges-Nojosa, D. M., & Maia, J. P. (2015). Prevalence and diversity of Hepatozoon in native and exotic geckos from Brazil. Journal of Parasitology, 101, 80–85.

    Article  PubMed  Google Scholar 

  • Harris, D. J., Graciá, E., Jorge, F., Maia, J. P. M. C., Perera, A., Carretero, M. A., & Giménez, A. (2013). Molecular detection of Hemolivia (Apicomplexa: Haemogregarinidae) from ticks of North African Testudo graeca (Testudines: Testudinidae) and an estimation of their phylogenetic relationships using 18S rRNA sequences. Comparative Parasitology, 80, 292–296.

    Article  Google Scholar 

  • Harris, D. J., Maia, J. P. M. C., & Perera, A. (2011). Molecular characterization of Hepatozoon species in reptiles from the Seychelles. Journal of Parasitology, 97, 106–110.

    Article  PubMed  Google Scholar 

  • Herbert, J. D. K., Godfrey, S. S., Bull, C. M., & Menz, R. I. (2010). Developmental stages and molecular phylogeny of Hepatozoon tuatarae, a parasite infecting the New Zealand tuatara, Sphenodon punctatus and the tick, Amblyomma sphenodonti. International Journal for Parasitology, 40, 1311–1315.

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.

    Article  CAS  PubMed  Google Scholar 

  • Karadjian, G., Chavatte, J.-M., & Landau, I. (2015). Systematic revision of the adeleid haemogregarines, with creation of Bartazoon n. g., reassignment of Hepatozoon argantis Garnham, 1954 to Hemolivia, and molecular data on Hemolivia stellata. Parasite, 22, 31.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maia, J. P., Harris, D. J., Carranza, S., & Goméz-Díaz, E. (2016). Assessing the diversity, host-specificity and infection patterns of apicomplexan parasites in reptiles from Oman, Arabia. Parasitology. doi:10.1017/S0031182016001372.

  • Maia, J. P. M. C., Perera, A., & Harris, D. J. (2012). Molecular survey and microscopic examination of Hepatozoon Miller, 1908 (Apicomplexa: Adeleorina) in lacertid lizards from the western Mediterranean. Folia Parasitologica, 59, 241–248.

    Article  PubMed  Google Scholar 

  • Moço, T. C., da Silva, R. J., Madeira, N. G., Dos Santos Paduan, K., Rubini, A. S., Leal, D. D. M., & O’Dwyer, L. H. (2012). Morphological, morphometric, and molecular characterization of Hepatozoon spp. (Apicomplexa, Hepatozoidae) from naturally infected Caudisona durissa terrifica (Serpentes, Viperidae). Parasitology Research, 110, 1393–1401.

    Article  PubMed  Google Scholar 

  • Morato, S. A. A., Lima, A. M. X., Staut, D. C. P., Faria, R. G., Souza-Alves, J. P., Gouveia, S. F., et al. (2011). Amphibians and reptiles of the Refúgio de Vida Silvestre Mata do Junco, municipality of Capela, state of Sergipe, northeastern Brazil. Check List, 7, 756–762.

    Article  Google Scholar 

  • Morrison, D. A. (2009). Evolution of the Apicomplexa: Where are we now? Trends in Parasitology, 25, 375–382.

    Article  PubMed  Google Scholar 

  • O’Dwyer, L. H., Moço, T. C., Paduan, K. D. S., Spenassatto, C., da Silva, R. J., & Ribolla, P. E. M. (2013). Description of three new species of Hepatozoon (Apicomplexa, Hepatozoidae) from Rattlesnakes (Crotalus durissus terrificus) based on molecular, morphometric and morphologic characters. Experimental Parasitology, 135, 200–207.

    Article  PubMed  Google Scholar 

  • Perkins, S. L., & Keller, A. K. (2001). Phylogeny of nuclear small subunit rRNA genes of hemogregarines amplified with specific primers. Journal of Parasitology, 87, 870–876.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D. (2008). jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Article  CAS  PubMed  Google Scholar 

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Telford, S. R. (2009). Hemoparasites of the Reptilia (p. 394). Boca Raton, Florida: CRC Press, Taylor and Francis.

    Google Scholar 

  • Tomé, B., Maia, J. P., Salvi, D., Brito, J. C., Carretero, M. A., Perera, A., et al. (2014). Patterns of genetic diversity in Hepatozoon spp. infecting snakes from North Africa and the Mediterranean Basin. Systematic Parasitology, 87, 249–258.

    Article  PubMed  Google Scholar 

  • Tomé, B., Rato, C., Perera, A., & Harris, D. J. (2016). High diversity of Hepatozoon spp. in geckos of the genus Tarentola. Journal of Parasitology, 102, 476–480.

    Article  PubMed  Google Scholar 

  • Uetz, P., & Hošek, J. (2015). The Reptile Database. http://www.reptile-database.org. Accessed 19 March 2016.

  • Ujvari, B., Madsen, T., & Olsson, M. (2004). High prevalence of Hepatozoon spp. (Apicomplexa, Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. Journal of Parasitology, 90, 670–672.

    Article  PubMed  Google Scholar 

  • Vitt, L. J., Caldwell, J. P., Colli, G. R., Garda, A. A., Mesquita, D. O., França, F. G. R., & Balbino, S. F. (2002). Um guia fotográfico dos répteis e anfíbios da região do Jalapão no Cerrado brasileiro. Publications in Herpetology Sam Noble Oklahoma Museum of Natural History, Norman, Oklahoma, USA, 1, 1–17.

    Google Scholar 

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Funding

This study was supported by CNPq to Project “Pesquisador Visitante Estrangeiro” (PVE-Process No.401800/2013-1). DMBNojosa was supported by CNPq “Pesquisador Produtividade” (PQ-Process No. 309617/20120). DJH was funded through an IF-FCT contract (IF/01627/2014) under the “Programa Operacional Potencial Humano – Quadro de Referência Estratégico Nacional” funds from the European Social Fund and the Portuguese Ministério da Educação e Ciência.

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Authors and Affiliations

  1. Núcleo Regional de Ofiologia da Universidade Federal do Ceará (NUROF-UFC), Campus do Pici, Centro de Ciências, Bloco 905, Pici, Fortaleza, CE, CEP 60.440-554, Brazil

    Diva M. Borges-Nojosa, M. Juliana Borges-Leite, Djan Zanchi-Silva & Roberta da Rocha Braga

  2. CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, No 7, 4485-661, Vairão, Vila do Conde, Portugal

    João P. Maia & D. James Harris

  3. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, R. Campo Alegre s/n, 4169-007, Porto, Portugal

    D. James Harris

Authors
  1. Diva M. Borges-Nojosa
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  2. M. Juliana Borges-Leite
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  3. João P. Maia
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  4. Djan Zanchi-Silva
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  5. Roberta da Rocha Braga
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  6. D. James Harris
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Corresponding author

Correspondence to D. James Harris.

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All applicable institutional, national and international guidelines for the care and use of animals were followed.

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Borges-Nojosa, D.M., Borges-Leite, M.J., Maia, J.P. et al. A new species of Hepatozoon Miller, 1908 (Apicomplexa: Adelerina) from the snake Philodryas nattereri Steindachner (Squamata: Dipsadidae) in northeastern Brazil. Syst Parasitol 94, 65–72 (2017). https://doi.org/10.1007/s11230-016-9676-2

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  • DOI: https://doi.org/10.1007/s11230-016-9676-2

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