Morphological and molecular characterization of Karyolysus--a neglected but common parasite infecting some European lizards
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
25492802
PubMed Central
PMC4298996
DOI
10.1186/s13071-014-0555-x
PII: s13071-014-0555-x
Knihovny.cz E-zdroje
- MeSH
- Coccidia cytologie genetika izolace a purifikace MeSH
- DNA helmintů chemie genetika MeSH
- fylogeneze MeSH
- ještěři parazitologie MeSH
- krev parazitologie MeSH
- mikroskopie MeSH
- molekulární sekvence - údaje MeSH
- protozoální DNA chemie genetika MeSH
- ribozomální DNA chemie genetika MeSH
- RNA ribozomální 18S genetika MeSH
- sekvenční analýza DNA MeSH
- shluková analýza MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Evropa MeSH
- Názvy látek
- DNA helmintů MeSH
- protozoální DNA MeSH
- ribozomální DNA MeSH
- RNA ribozomální 18S MeSH
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.
Institute of Parasitology Slovak Academy of Sciences Hlinkova 3 040 01 Košice Slovak Republic
Institute of Zoology Poznań University of Life Sciences Wojska Polskiego 71 C 60 625 Poznań Poland
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Telford SR. Hemoparasites of Reptilia, Color Atlas and Text. Boca Raton, Florida, USA: CRC Press, Taylor & Francis Group; 2009.
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. doi: 10.1007/s00436-008-0912-9. PubMed DOI
Hassl AR. Blood parasitism by hemogregarines in Central European lizards. Herpetozoa. 2012;25(1–2):83–86.
Svahn K. Blood parasites of the genus Karyolysus (Coccidia, Adeleidae) in Scandinavian lizards. Description and life cycle. Norw J Zool. 1975;23:277–295.
Svahn K. Incidence of blood parasites of the genus Karyolysus (Coccidia) in Scandinavian lizards. Oikos. 1974;25:43–53. doi: 10.2307/3543544. DOI
Beyer TV, Sidorenko NV. Karyolysus sp. (Haemogregarinidae, Adeleida, Apicomplexa): Host-Parasite Relationships of Persisting Stages. J Protozool. 1984;31(4):513–517. doi: 10.1111/j.1550-7408.1984.tb05493.x. DOI
Gwiazdowicz DJ, Filip KP. Ophionyssus saurarum (Acari, Mesostigmata) infecting Lacerta agilis (Reptilia, Lacertidae) Wiad Parazytol. 2009;55(1):61–62. PubMed
Siuda K. Kleszcze (Acari: Ixodida) Polski. I. Warszawa: Wiadomości ogólne; 1991.
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. doi: 10.1007/s00436-010-1981-0. PubMed DOI
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. doi: 10.1645/GE-1330.1. PubMed DOI
Garrido M, Perez-Mellado V. Prevalence and intensity of blood parasites in insular lizards. Zool Anz. 2013;252(4):588–592. doi: 10.1016/j.jcz.2012.11.003. DOI
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. doi: 10.1007/s00436-005-1355-1. PubMed DOI
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. doi: 10.1007/s00436-004-1212-7. PubMed DOI
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. doi: 10.1007/s00436-005-1354-2. PubMed DOI
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. doi: 10.1007/s00114-013-1051-4. PubMed DOI
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. doi: 10.1007/s11230-009-9206-6. PubMed DOI
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. doi: 10.1645/JP-GE-2908.1. PubMed DOI
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. doi: 10.14411/fp.2012.033. PubMed DOI
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. doi: 10.1111/j.1550-7408.2011.00607.x. PubMed DOI
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. doi: 10.1645/13-203.1. PubMed DOI
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. doi: 10.1016/j.protis.2014.06.001. PubMed DOI
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. doi: 10.1007/s11230-014-9477-4. PubMed DOI
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. doi: 10.1603/0022-2585(2007)44[869:MIOBSI]2.0.CO;2. PubMed DOI
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. doi: 10.1645/GE-204R. PubMed DOI
Perkins SL, Keller AK. Phylogeny of nuclear small subunit rRNA genes of hemogregarines amplified with specific primers. J Parasitol. 2001;87(4):870–876. doi: 10.1645/0022-3395(2001)087[0870:PONSSR]2.0.CO;2. PubMed DOI
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. doi: 10.1093/sysbio/syq010. PubMed DOI
Felsenstein J. Confidence-Limits on Phylogenies - an Approach Using the Bootstrap. Evolution. 1985;39(4):783–791. doi: 10.2307/2408678. PubMed DOI
Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. doi: 10.1093/bioinformatics/14.9.817. PubMed DOI
Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8):754–755. doi: 10.1093/bioinformatics/17.8.754. PubMed DOI
Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16(1):37–48. doi: 10.1093/oxfordjournals.molbev.a026036. PubMed DOI
Maia JP, Harris DJ, Perera A. Molecular survey of Hepatozoon species in lizards from North Africa. J Parasitol. 2011;97(3):513–517. doi: 10.1645/GE-2666.1. PubMed DOI
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. doi: 10.1017/S0031182013001649. PubMed DOI
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. doi: 10.1186/1756-3305-6-102. PubMed DOI PMC
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. doi: 10.1654/4594.1. DOI
Siddall ME. Phylogeny of adeleid blood parasites with a partial systematic revision of the haemogregarine complex. J Eukaryot Microbiol. 1995;42(2):116–125. doi: 10.1111/j.1550-7408.1995.tb01551.x. PubMed DOI
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. doi: 10.1645/0022-3395(2000)086[0451:IDOSOH]2.0.CO;2. PubMed DOI
Smith TG. The genus Hepatozoon (Apicomplexa: Adeleina) J Parasitol. 1996;82(4):565–585. doi: 10.2307/3283781. PubMed DOI
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. doi: 10.1645/0022-3395(2001)087[0606:TOHCTD]2.0.CO;2. PubMed DOI
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. doi: 10.1016/j.vetpar.2009.05.028. PubMed DOI
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. doi: 10.1016/j.vetpar.2013.02.017. PubMed DOI
GENBANK
KJ461939, KJ461940, KJ461941, KJ461942, KJ461943, KJ461944, KJ461945, KJ461946