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Morphometric and molecular characterisation of Hepatozoon bashtari n. sp. in painted saw-scaled viper, Echis coloratus (Ophidia, Viperidae)

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Abstract

Hepatozoon species are the most widely known haemogregarines infecting a wide range of vertebrates, although predominately snakes. Herein, Hepatozoon bashtari n. sp., originally infecting the painted saw-scaled viper, Echis coloratus, in Saudi Arabia is described using both morphological features and molecular data from 18S rDNA sequences. The overall prevalence of infection was 60% (9/15) with parasitaemia ranging from 52 to 60%. Gamonts were entirely intraerythrocytic and were observed to cause considerable hypertrophy within the host cell. The mean size of mature gamonts was 15.4 × 3.3 μm. Merogonic stages were confined to the lung endothelial cells with monomorphic meronts. The average size of mature meronts was 32 × 12 μm and they were estimated to produce 13–16 merozoites each. The phylogenetic tree generated from SSU rDNA sequences revealed that Hepatozoon bashtari sp. n. clusters with the vast majority of other Hepatozoon species infecting snakes, lizards and geckos in various regions of the world, which would appear to support the hypothesis of prey-predator transmission of the genus Hepatozoon. Through a combination of morphological comparison with closely related Hepatozoon spp. and 18S rRNA gene sequence analysis, it is possible to confirm Hepatozoon bashtari sp. n. as a new species.

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References

  • Abdel-Baki AS, Al-Quraishy S, Zhang JY (2014) Redescription of Haemogregarina garnhami (Apicomplexa: Adeleorina) from the blood of Psammophis schokari (Serpentes: Colubridae) as Hepatozoon garnhami n. comb. based on molecular, morphometric and morphologic characters. Acta Parasitol 59:294–300

    Article  Google Scholar 

  • Abdel-Haleem HM, Mansour L, Holal M, Qasem MA, Al-Quraishy S, Abdel-Baki AS (2018) Molecular characterisation of Hepatozoon aegypti Bashtar, Boulos & Mehlhorn, 1984 parasitising the blood of Spalerosophis diadema (Serpentes: Colubridae). Parasitol Res 117:3119–3125. https://doi.org/10.1007/s00436-018-6006-4

    Article  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  • Arnold EN, Robinson MD, Carranza S (2009) A preliminary analysis of phylogenetic relationships and biogeography of the dangerously venomous Carpet Vipers, Echis (Squamata, Serpentes, Viperidae) based on mitochondrial DNA sequences. Amphibia-Reptilia 30:273–282

    Article  Google Scholar 

  • Ball GH, Chao J, Smith SR (1967) The life history of Hepatozoon rarefaciens (Sambon and Seligmann, 1907) from Drymarchon corais (Colubridae), and its experimental transfer to Constrictor constrictor (Boidae). J Parasitol 53:897–909

    Article  CAS  Google Scholar 

  • Barta JR, Ogedenbre JD, Martin DS, Smith TG (2012) Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rDNA sequences. J Eukaryot Microbiol 59:171–180

    Article  CAS  Google Scholar 

  • Bashtar AR, Boulos R, Mehlhorn H (1984) Hepatozoon aegypti nov. sp. 1. Life cycle. Z Parasitenkd 70:29–41

    Article  Google Scholar 

  • Bashtar AR, Abdel-Ghaffar FA, Shazly MA (1991) Life cycle of Hepatozoon mehlhorni sp. nov. in the viper Echis carinatus and the mosquito Culex pipiens. Parasitol Res 77:402–410

    Article  CAS  Google Scholar 

  • Cook CA, Smit NJ, Davies AJ (2010) Hemoproteids (Apicomplexa: Haemoproteidae) from South African tortoises (Cryptodira: Testudinidae). J Parasitol 96:1168–1172

    Article  CAS  Google Scholar 

  • Cook CA, Lawton SP, Davies AJ, Smit NJ (2014) Reassignment of the land tortoise haemogregarine Haemogregarina fitzsimonsi Dias 1953 (Adeleorina: Haemogregarinidae) to the genus Hepatozoon Miller 1908 (Adeleorina: Hepatozoidae) based on parasite morphology, life cycle and phylogenetic analysis of 18S rDNA sequence fragments. Parasitology 141:1611–1620. https://doi.org/10.1017/S003118201400081X

  • Cook CA, Netherlands EC, Smit NJ (2015) First Hemolivia from Southern Africa: reassigning chelonian Haemogregarina parvula Dias, 1953 (Adeleorina: Haemogregarinidae) to Hemolivia (Adeleorina: Karyolysidae). Afr Zool 50:165–173

    Article  Google Scholar 

  • Cook CA, Netherlands EC, As JV, Jacobus Smit N (2018) Two new species of Hepatozoon (Apicomplexa: Hepatozoidae) parasitising species of Philothamnus (Ophidia: Colubridae) from South Africa. Folia Parasitol 65

  • Das I (2016) A field guide to the reptiles of South-East Asia. Bloomsbury Natural History, New York

    Google Scholar 

  • Dvořáková N, Kvičerová J, Papoušek I, Javanbakht H, Tiar G, Kami H, Široký P (2014) Haemogregarines from western Palaearctic freshwater turtles (genera Emys, Mauremys) are conspecific with Haemogregarina stepanowi Danilewsky, 1885. Parasitology 141:522–530

    Article  Google Scholar 

  • Fischer AH, Jacobson KA, Rose J, Zeller R (2008) Hematoxylin and eosin staining of tissue and cell sections. CSH Protoc 2008:pdb.prot 4986

    Google Scholar 

  • Guindon S, Dufayard JF, 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. Syst Biol 59:307–321

    Article  CAS  Google Scholar 

  • Hall T (2001) BioEdit Version 5.0.6. North Carolina State University, Raleigh

    Google Scholar 

  • Han H, Wu Y, Dong H, Zhu S, Li L, Zhao Q, Wu D, Pei E, Wang Y, Huang B (2015) First report of Hepatozoon (Apicomplexa: Adeleorina) from king ratsnakes (Elaphe carinata) in Shanghai, with description of a new species. Acta Parasitol 60:266–274

    Article  Google Scholar 

  • Hoare CA (1932) On protozoal blood parasites collected in Uganda. With an account of the life cycle of the crocodile haemogregarine. Parasitology 24:210–224

    Article  Google Scholar 

  • Lainson R, Paperna I, Naiff RD (2003) Development of Hepatozoon caimani (Carini, 1909) Pess A, De Biasi & De Souza, 1972 in the Caiman Caiman c. crocodilus, the frog Rana catesbeiana and the mosquito Culex fatigans. Mem Inst Oswaldo Cruz 98:103–113

    Article  Google Scholar 

  • Larkin EK, Morris NJ, Li Y, Nock NL, Stein CM (2007) Comparison of affected sibling-pair linkage methods to identify gene x gene interaction in GAW15 simulated data. BMC Proc Suppl 1:S66

    Article  Google Scholar 

  • Maia JP, Harris DJ, Perera A (2011) Molecular survey of Hepatozoon species in lizards from North Africa. J Parasitol 97:513–517

    Article  Google Scholar 

  • Maia JP, Crottini A, Harris DJ (2014) Microscopic and molecular characterization of Hepatozoon domerguei (Apicomplexa) and Foleyella furcata (Nematoda) in wild endemic reptiles from Madagascar. Parasite 21:47

    Article  Google Scholar 

  • Maia JP, Carranza S, Harris DJ (2016) Comments on the systematic revision of adeleid haemogregarines: Are more data needed? J Parasitol 102:549–552. https://doi.org/10.1645/15-930

  • Mallow D, Ludwig D, Nilson G (2003) True vipers: natural history and taxonomy of old world vipers, first edn. Krieger Publishing Company, Malabar

    Google Scholar 

  • McDiarmid RW, Campbell JA, Touré TA (1999) Snake species of the world: a taxonomic and geographic reference. v. 1. Herpetologists’ League, Washington, DC

    Google Scholar 

  • Mercer SH, Craig TM (1988) Comparison of various staining procedures in the identification of Hepatozoon canis gamonts. Vet Clin Pathol 17:63–65

    Article  CAS  Google Scholar 

  • Mohiuddin A, Pal RA, Warsi AA (1967) Haemogregarina echisi n. sp. from the saw-scaled viper Echis carinatus of the Sind Region of West Pakistan. J Protozool 14:255–259

    Article  Google Scholar 

  • Perkins SL, Keller AK (2001) Phylogeny of nuclear small subunit rRNA genes of hemogregarines amplified with specific primers. J Parasitol 87:870–876

    Article  CAS  Google Scholar 

  • Rhadi AF, Rastegar-Pouyani N, Mohammed GR, Al-Fartosi KH, Browne RK, Karamiani R (2015) A study of the Nomino typic form of saw scaled viper, Echis carinatus, (Schneider 1801), (Squamata: Ophidia: Viperidae) in Southern Iraq. Sch Acad J Biosci 3:845–851

    Google Scholar 

  • Robin LA (1936) Cycle évolutif d’un Hepatozoon de Gecko verticillatus. Ann Inst Pasteur Paris 56:376–394

    Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  Google Scholar 

  • Saoud M, Ramadan N, Mohammed S, Fawzi S (1996) On two new haemogregarines (Protozoa: Apicomplexa) from Colubrid and Elapidae snakes in Egypt. Qatar Univ Sci J 16:127–139

  • Smith TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). J Parasitol 82:565–585

    Article  CAS  Google Scholar 

  • Smith TG, Desser SS (1997) Phylogenetic analysis of the genus Hepatozoon Millet 1908 (Apicomplexa: Adeleorina). Syst Parasitol 36:213–221

    Article  Google Scholar 

  • Smith TG, Desser SS, Martin DS (1994) The development of Hepatozoon sipedon sp. nov. (Apicomplexa: Adeleina: Hepatozoidae) in its natural host, the Northern water snake (Nerodia sipedon sipedon), in the culicine vectors Culex pipiens and C. territans, and in an intermediate host, the Northern leopard frog (Rana pipiens). Parasitol Res 80:559–568

  • Stümpel N, Joger U (2009) Recent advances in phylogeny and taxonomy of Near and Middle Eastern Vipers - an update. ZooKeys 31:179–191

    Article  Google Scholar 

  • Telford SR (2009) Hemoparasites of the Reptilia: color atlas and text, 1st edn. CRC Press, Taylor and Francis Group, Boca Raton

    Google Scholar 

  • Telford SR Jr, Moler PE, Butler JF (2012) Four additional Hepatozoon species (Apicomplexa: Hepatozoidae) from north Florida ratsnakes, genus Pantherophis. Folia Parasitol 59:167–172. https://doi.org/10.14411/fp.2012.023

  • Tomé B, Maia JP, Harris DJ (2012) Hepatozoon infection prevalence in four snake genera: influence of diet, prey parasitemia levels or parasite type? J Parasitol 98:913–917

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ujvari B, Madsen T, Olsson M (2004) High prevalence of Hepatozoon spp. (Apicomplexa, Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. J Parasitol 90:670–267

    Article  Google Scholar 

  • Úngari LP, Santos AL, O'Dwyer LH, da Silva MRL, de Melo Fava NN, Paiva GCM, Pinto R, Cury MC (2018) Haemogregarina podocnemis sp. nov.: description of a new species of Haemogregarina Danilewsky 1885 (Adeleina: Haemogregarinaidae) in free-living and captive yellow-spotted river turtles Podocnemis unifilis (Testudines: Podocnemididae) from Brazil. Parasitol Res 117:1535–1548

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This work was supported by the Researcher supporting Project (RSP-2019/3), King Saud University.

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Correspondence to Abdel-Azeem S. Abdel-Baki.

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Abdel-Baki, AA.S., Mansour, L., Al-Malki, E.S. et al. Morphometric and molecular characterisation of Hepatozoon bashtari n. sp. in painted saw-scaled viper, Echis coloratus (Ophidia, Viperidae). Parasitol Res 119, 3793–3801 (2020). https://doi.org/10.1007/s00436-020-06886-y

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