Particle and Fibre Toxicology | |
Morphological and molecular characterization of Karyolysus – a neglected but common parasite infecting some European lizards | |
Viktória Majláthová7  Beáta Malčeková1  Natália Kokošová4  Piotr Tryjanowski6  Gábor Földvári3  David James Harris5  Karol Račka2  Igor Majláth4  Adriana Hižňanová4  Božena Haklová-Kočíková7  | |
[1] Department of Biochemical Sciences, Charles University in Prague, Faculty of Pharmacy in Hradec Kralove, Hradec Kralove, Czech Republic;Department of Parasitology, State Veterinary Institute Jihlava, Rantířovská 93, Jihlava, 586 05, Czech Republic;Department of Parasitology and Zoology, Faculty of Veterinary Science, Szent István University, 2 István Street, Budapest H-1078, Hungary;Institute of Biology and Ecology, University of P. J. Šafárik in Košice, Moyzesova 11, Košice, 040 01, Slovak Republic;CI-BIO-UP, Centro de Investigação em Biodiversidade e Recursors Genéticos da Universidade do Porto, Campus Agrário de Vairão, Vairão, 4485-661, Portugal;Institute of Zoology, Poznań University of Life Sciences, Wojska Polskiego 71 C, Poznań, 60-625, Poland;Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, Košice, 040 01, Slovak Republic | |
关键词: Europe; lizards; Lacertidae; Ophionyssus; Karyolysus; | |
Others : 1148676 DOI : 10.1186/s13071-014-0555-x |
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received in 2014-08-07, accepted in 2014-11-22, 发布年份 2014 | |
【 摘 要 】
Background
Blood parasites of the genus Karyolysus Labbé, 1894 (Apicomplexa: Adeleida: Karyolysidae) represent the protozoan haemogregarines found in various genera of lizards, including Lacerta, Podarcis, Darevskia (Lacertidae) and Mabouia (Scincidae). The vectors of parasites are gamasid mites from the genus Ophionyssus.
Methods
A total of 557 individuals of lacertid lizards were captured in four different localities in Europe (Hungary, Poland, Romania and Slovakia) and blood was collected. Samples were examined using both microscopic and molecular methods, and phylogenetic relationships of all isolates of Karyolysus sp. were assessed for the first time. Karyolysus sp. 18S rRNA isolates were evaluated using Bayesian and Maximum Likelihood analyses.
Results
A total of 520 blood smears were examined microscopically and unicellular protozoan parasites were found in 116 samples (22.3% prevalence). The presence of two Karyolysus species, K. latus and K. lacazei was identified. In total, of 210 samples tested by polymerase chain reaction (PCR), the presence of parasites was observed in 64 individuals (prevalence 30.5%). Results of phylogenetic analyses revealed the existence of four haplotypes, all part of the same lineage, with other parasites identified as belonging to the genus Hepatozoon.
Conclusions
Classification of these parasites using current taxonomy is complex - they were identified in both mites and ticks that typically are considered to host Karyolysus and Hepatozoon respectively. Furthermore although distortions to the intermediate host erythrocyte nuclei were observed, the defining characteristic of Karyolysus, the haplotypes were nearly identical to those reported from lizards in the Iberian Peninsula, where such distortions were not reported and which were thus identified as Hepatozoon. Based on the phylogenetic analyses, neither vertebrate host, nor geographical patterns of the studied blood parasites could be established.
【 授权许可】
2014 Haklová-Kocíková et al.; licensee BioMed Central.
【 预 览 】
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Figure 1. | 45KB | Image | download |
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【 参考文献 】
- [1]Telford SR: Hemoparasites of Reptilia, Color Atlas and Text. CRC Press, Taylor & Francis Group, Boca Raton, Florida, USA; 2009.
- [2]Mihalca AD, Racka K, Gherman C, Ionescu DT: Prevalence and intensity of blood apicomplexan infections in reptiles from Romania. Parasitol Res 2008, 102(5):1081-1083.
- [3]Hassl AR: Blood parasitism by hemogregarines in Central European lizards. Herpetozoa 2012, 25(1–2):83-86.
- [4]Svahn K: Blood parasites of the genus Karyolysus (Coccidia, Adeleidae) in Scandinavian lizards. Description and life cycle. Norw J Zool 1975, 23:277-295.
- [5]Svahn K: Incidence of blood parasites of the genus Karyolysus (Coccidia) in Scandinavian lizards. Oikos 1974, 25:43-53.
- [6]Beyer TV, Sidorenko NV: Karyolysus sp. (Haemogregarinidae, Adeleida, Apicomplexa): Host-Parasite Relationships of Persisting Stages. J Protozool 1984, 31(4):513-517.
- [7]Gwiazdowicz DJ, Filip KP: Ophionyssus saurarum (Acari, Mesostigmata) infecting Lacerta agilis (Reptilia, Lacertidae). Wiad Parazytol 2009, 55(1):61-62.
- [8]Siuda K: Kleszcze (Acari: Ixodida) Polski. I. Wiadomości ogólne, Warszawa; 1991.
- [9]Majlathova V, Majlath I, Haklova B, Hromada M, Ekner A, Antczak M, Tryjanowski P: Blood parasites in two co-existing species of lizards (Zootoca vivipara and Lacerta agilis). Parasitol Res 2010, 107(5):1121-1127.
- [10]Telford SR, Moler PE, Butlert JF: Hepatozoon species of the timber rattlesnake in northern Florida: Description of a new species, evidence of salivary gland oocysts, and a natural cross-familial transmission of an Hepatozoon species. J Parasitol 2008, 94(2):520-523.
- [11]Garrido M, Perez-Mellado V: Prevalence and intensity of blood parasites in insular lizards. Zool Anz 2013, 252(4):588-592.
- [12]Amo L, Fargallo JA, Martinez-Padilla J, Millan J, Lopez P, Martin J: Prevalence and intensity of blood and intestinal parasites in a field population of a Mediterranean lizard, Lacerta lepida. Parasitol Res 2005, 96(6):413-417.
- [13]Amo L, Lopez P, Martin J: Prevalence and intensity of haemogregarinid blood parasites in a population of the Iberian rock lizard, Lacerta monticola. Parasitol Res 2004, 94(4):290-293.
- [14]Amo L, Lopez P, Martin J: Prevalence and intensity of haemogregarine blood parasites and their mite vectors in the common wall lizard, Podarcis muralis. Parasitol Res 2005, 96(6):378-381.
- [15]Molnar O, Bajer K, Meszaros B, Torok J, Herczeg G: Negative correlation between nuptial throat colour and blood parasite load in male European green lizards supports the Hamilton-Zuk hypothesis. Naturwissenschaften 2013, 100(6):551-558.
- [16]Roca V, Galdon MA: Haemogregarine blood parasites in the lizards Podarcis bocagei (Seoane) and P. carbonelli (Perez-Mellado) (Sauria: Lacertidae) from NW Portugal. Syst Parasitol 2010, 75(1):75-79.
- [17]Harris DJ, Maia JPMC, Perera A: Molecular Survey of Apicomplexa in Podarcis Wall Lizards Detects Hepatozoon, Sarcocystis, and Eimeria Species. J Parasitol 2012, 98(3):592-597.
- [18]Maia JPMC, Perera A, Harris DJ: Molecular survey and microscopic examination of Hepatozoon Miller, 1908 (Apicomplexa: Adeleorina) in lacertid lizards from the western Mediterranean. Folia Parasit 2012, 59(4):241-248.
- [19]Barta JR, Ogedengbe JD, Martin DS, Smith TG: Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18s rDNA sequences. J Euk Microbiol 2012, 59(2):171-180.
- [20]Harris DJ, Damas-Moreira I, Maia JPMC, Perera A: First report of Hepatozoon (Apicomplexa: Adeleorina) in caecilians, with description of a new species. J Parasitol 2014, 100(1):117-120.
- [21]Kvičerová J, Hypša V, Dvořáková N, Mikulíček P, Jandzik D, Gardner MG, Javanbakht H, Tiar G, Široký P: Hemolivia and Hepatozoon: Haemogregarines with tangled evolutionary relationships. Protist 2014, 165(5):688-700.
- [22]Tomé B, Maia JP, Salvi D, Brito JC, Carretero MA, Perera A, Meimberg H, Harris DJ: Patterns of genetic diversity in Hepatozoon spp. infecting snakes from North Africa and the Mediterranean Basin. Syst Parasitol 2014, 87(3):249-258.
- [23]Humair PF, Douet V, Cadenas FM, Schouls LM, Van de Pol I, Gern L: Molecular identification of bloodmeal source in Ixodes ricinus ticks using 12S rDNA as a genetic marker. J Med Entomol 2007, 44(5):869-880.
- [24]Ujvari B, Madsen T, Olsson M: High prevalence of Hepatozoon spp. (Apicomplexa, hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. J Parasitol 2004, 90(3):670-672.
- [25]Perkins SL, Keller AK: Phylogeny of nuclear small subunit rRNA genes of hemogregarines amplified with specific primers. J Parasitol 2001, 87(4):870-876.
- [26]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol 2010, 59(3):307-321.
- [27]Felsenstein J: Confidence-Limits on Phylogenies - an Approach Using the Bootstrap. Evolution 1985, 39(4):783-791.
- [28]Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14(9):817-818.
- [29]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17(8):754-755.
- [30]Bandelt HJ, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16(1):37-48.
- [31]Maia JP, Harris DJ, Perera A: Molecular survey of Hepatozoon species in lizards from North Africa. J Parasitol 2011, 97(3):513-517.
- [32]Quillfeldt P, Martínez J, Bugoni L, Mancini PL, Merino S: Blood parasites in noddies and boobies from Brazilian offshore islands-differences between species and influence of nesting habitat. Parasitology 2014, 141(3):399-410.
- [33]Baneth G, Sheiner A, Eyal O, Hahn S, Beaufils JP, Anug Y, Talmi-Frank D: Redescription of Hepatozoon felis (Apicomplexa: Hepatozoidae) based on phylogenetic analysis, tissue and blood form morphology, and possible transplacental transmission. Parasit Vectors 2013, 6:102. BioMed Central Full Text
- [34]Harris DJ, Graciá E, Jorge F, Maia JPMC, Perera A, Carretero MA, Giménez A: Molecular Detection of Hemolivia (Apicomplexa: Hameogregarinidae) from Ticks of North African Testudo graeca (Testudines: Testudinidae) and an Estimation of Their Phylogenetic Relationships Using 18S rRNA Sequences. Comp Parasitol 2013, 80(2):292-296.
- [35]Siddall ME: Phylogeny of adeleid blood parasites with a partial systematic revision of the haemogregarine complex. J Eukaryot Microbiol 1995, 42(2):116-125.
- [36]Smith TG, Kim B, Hong H, Desser SS: Intraerythrocytic development of species of Hepatozoon infecting ranid frogs: evidence for convergence of life cycle characteristics among apicomplexans. J Parasitol 2000, 86(3):451-458.
- [37]Smith TG: The genus Hepatozoon (Apicomplexa: Adeleina). J Parasitol 1996, 82(4):565-585.
- [38]Baneth G, Samish M, Alekseev E, Aroch I, Shkap V: Transmission of Hepatozoon canis to Dogs by Naturally-Fed or Percutaneously-Injected Rhipicephalus sanguineus Ticks. J Parasitol 2001, 87(3):606-611.
- [39]Johnson EM, Allen KE, Panciera RJ, Ewing SA, Little SE: Experimental transmission of Hepatozoon americanum to New Zealand White rabbits (Oryctolagus cuniculus) and infectivity of cystozoites for a dog. Vet Parasitol 2009, 164(2–4):162-166.
- [40]Giannelli A, Ramos RAN, Di Paola G, Mencke N, Torres FD, Baneth G, Otranto D: Transstadial transmission of Hepatozoon canis from larvae to nymphs of Rhipicephalus sanguineus. Vet Parasitol 2013, 196(1–2):1-5.