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Molecular phylogenetic analysis in Hammondia-like organisms based on partial Hsp70 coding sequences

Published online by Cambridge University Press:  27 April 2007

R. M. MONTEIRO
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil
L. J. RICHTZENHAIN
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil
H. F. J. PENA
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil
S. L. P. SOUZA
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil
M. R. FUNADA
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil
S. M. GENNARI
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil
J. P. DUBEY
Affiliation:
Animal Parasitic Diseases Laboratory, Animal and Natural Resources Institute, Agricultural Research Service, United States Department of Agricultural, Building 1001, Beltsville, MD 20705, USA
C. SREEKUMAR
Affiliation:
Animal Parasitic Diseases Laboratory, Animal and Natural Resources Institute, Agricultural Research Service, United States Department of Agricultural, Building 1001, Beltsville, MD 20705, USA
L. B. KEID
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil
R. M. SOARES*
Affiliation:
Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil
*
*Corresponding author: Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo. Av. Prof. Dr. Orlando Marques de Paiva, 87, CEP 05508-900, São Paulo, SP, Brazil. Tel: +55 11 3091 1392. Fax: +55 11 3091 1392. E-mail: rosoares@usp.br

Summary

The 70 kDa heat-shock protein (Hsp70) sequences are considered one of the most conserved proteins in all domains of life from Archaea to eukaryotes. Hammondia heydorni, H. hammondi, Toxoplasma gondii, Neospora hughesi and N. caninum (Hammondia-like organisms) are closely related tissue cyst-forming coccidians that belong to the subfamily Toxoplasmatinae. The phylogenetic reconstruction using cytoplasmic Hsp70 coding genes of Hammondia-like organisms revealed the genetic sequences of T. gondii, Neospora spp. and H. heydorni to possess similar levels of evolutionary distance. In addition, at least 2 distinct genetic groups could be recognized among the H. heydorni isolates. Such results are in agreement with those obtained with internal transcribed spacer-1 rDNA (ITS-1) sequences. In order to compare the nucleotide diversity among different taxonomic levels within Apicomplexa, Hsp70 coding sequences of the following apicomplexan organisms were included in this study: Cryptosporidium, Theileria, Babesia, Plasmodium and Cyclospora. Such analysis revealed the Hammondia-like organism to be the lowest divergent group when compared to other groups within the phylum Apicomplexa. In conclusion, the Hsp70 coding sequences proved to be a valuable genetic marker for phylogenetic reconstruction and may constitute a good candidate to be used with other genes for species phylogeny within this group of organisms.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Abel, J., Schares, G., Orzeszko, K., Gasser, R. B. and Ellis, J. T. (2006). Hammondia isolated from dogs and foxes are genetically distinct. Parasitology 132, 187192.CrossRefGoogle ScholarPubMed
Budin, K. and Philippe, H. (1998). New insights into the phylogeny of eukaryotes based on ciliate Hsp70 sequences. Molecular Biology and Evolution 15, 943956.CrossRefGoogle ScholarPubMed
Bukau, B. and Horwich, A. L. (1998). The Hsp70 and Hsp60 Chaperone Machines. Cell 92, 351366.CrossRefGoogle ScholarPubMed
Dubey, J. P., Barr, B. C., Barta, J. R., Bjerkas, I., Björkman, C., Blagburn, B. L., Bowman, D. D., Buxton, D., Ellis, J. T., Gottstein, B., Hemphill, A., Hill, D. E., Howe, D. K., Jenkins, M. C., Kobayashi, Y., Koudela, B., Marsh, A. E., Mattsson, J. G., McAllister, M. M., Modry, D., Omata, Y., Sibley, L. D., Speer, C. A., Trees, A. J., Uggla, A., Upton, S. J., Williams, D. J. L. and Lindsay, D. S. (2002). Redescription of Neospora caninum and its differentiation from related coccidia. International Journal for Parasitology 32, 929946.CrossRefGoogle ScholarPubMed
Dubey, J. P., Liddell, S., Mattson, D., Speert, C. A., Howe, D. K. and Jenkins, M. C. (2001). Characterization of the Oregon isolate of Neospora hughesi from a horse. Journal of Parasitology 87, 345353.CrossRefGoogle ScholarPubMed
Ellis, J. T., Morrison, D. A., Liddell, S., Jenkins, M. C., Mohammed, O. B., Ryce, C. and Dubey, J. P. (1999). The genus Hammondia is paraphyletic. Parasitology 118, 357362.CrossRefGoogle ScholarPubMed
Fast, N. M., Xue, L., Bingham, S. and Keeling, P. J. (2002). Re-examining alveolate evolution using multiple protein molecular phylogenies. Journal of Eukaryotic Microbiology 49, 3037.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1978). Cases in which parsimony or compatibility methods will be positively misleading. Systematic Zoology 27, 401410.CrossRefGoogle Scholar
Frenkel, J. K. and Dubey, J. P. (1975). Hammondia hammondi gen nov., sp. nov., from domestic cats, a new coccidian related to Toxoplasma and Sarcocystis. Zeitschrift für Parasitenkunde 46, 312.CrossRefGoogle ScholarPubMed
Gondim, L. F. P., McAllister, M. M., Pitt, W. C. and Zemlicka, D. E. (2004). Coyotes (Canis latrans) are definitive hosts of Neospora caninum. International Journal for Parasitology 34, 159161.CrossRefGoogle ScholarPubMed
Gupta, R. S. and Golding, G. B. (1993). Evolution of the Hsp70 gene and its implications regarding relationships between Archaebacteria, Eubacteria, and Eukaryotes. Journal of Molecular Evolution 37, 573582.CrossRefGoogle ScholarPubMed
Gupta, R. S. (1998). Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiology and Molecular Biology Reviews 62, 14351491.CrossRefGoogle ScholarPubMed
Hoelzer, G. A. and Melnick, D. J. (1994). Patterns of speciation and limits to phylogenetic resolution. Tree 9, 104107.Google ScholarPubMed
Heydorn, A. O. and Mehlhorn, H. (2002). Neospora caninum is an invalid species name: an evaluation of facts and statements. Parasitology Research 88, 175184.CrossRefGoogle ScholarPubMed
Jenkins, M. C., Ellis, J. T., Liddell, S., Ryce, C., Munday, B. L., Morrison, D. A. and Dubey, J. P. (1999). The relationship of Hammondia hammondi and Sarcocystis mucosa to other heteroxenous cyst-forming coccidia as inferred by phylogenetic analysis of the 18S SSU ribosomal DNA sequence. Parasitology 119, 135142.CrossRefGoogle ScholarPubMed
Karlin, S. and Brocchieri, L. (1998). Heat shock protein 70 family: multiple sequence comparisons, function, and evolution. Journal of Molecular Evolution 47, 565577.CrossRefGoogle ScholarPubMed
Lindsay, D. S., Dubey, J. P. and Duncan, R. B. (1999). Confirmation that the dog is a defnitive host for Neospora caninum. Veterinary Parasitology 82, 327333.CrossRefGoogle Scholar
Lindsay, D. S., Ritter, D. M. and Brake, D. (2001). Oocyst excretion in dogs fed mouse brains containing tissue cysts of a cloned line of Neospora caninum. Journal of Parasitology 87, 909911.CrossRefGoogle ScholarPubMed
Lyons, R. E. and Johnson, A. M. (1998). Gene sequence and transcription differences in 70 kDa heat shock protein correlate with murine virulence of Toxoplasma gondii. International Journal for Parasitology 28, 10411051.CrossRefGoogle ScholarPubMed
McAllister, M. M., Dubey, J. P., Lindsay, D. S., Jolley, W. R., Wills, R. A. and McGuire, A. M. (1998). Dogs are definitive hosts of Neospora caninum. International Journal for Parasitology 28, 14731478.CrossRefGoogle ScholarPubMed
Morrison, D. A., Bornstein, S., Thebo, P., Wernery, U., Kinne, J. and Mattsson, J. G. (2004). The current status of the small subunit rRNA phylogeny of the coccidian (Sporozoa). International Journal for Parasitology 34, 501514.CrossRefGoogle ScholarPubMed
Mugridge, N. B., Morrison, D. A., Heckeroth, A. R., Johnson, A. M. and Tenter, A. M. (1999). Phylogenetic analysis based on full-length large subunit ribosomal RNA gene sequence comparison reveals that Neospora caninum is more closely related to Hammondia heydorni than to Toxoplasma gondii. International Journal for Parasitology 29, 15451556.CrossRefGoogle ScholarPubMed
Mugridge, N. B., Morrison, D. A., Jakel, T., Heckeroth, A. R., Tenter, A. M. and Johnson, A. M. (2000). Effects of sequence alignment and structural domains of ribosomal DNA on phylogeny reconstruction for the protozoan family sarcocystidae. Molecular Biology and Evolution 17, 18421853.CrossRefGoogle ScholarPubMed
Page, R. D. M. (1996). TREEVIEW: An application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357358.Google ScholarPubMed
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Rodrigues, A. A., Gennari, S. M., Aguiar, D. M., Sreekumar, C., Hill, D. E., Miska, K. B., Vianna, M. C. and Dubey, J. P. (2004). Shedding of Neospora caninum oocysts by dogs fed tissues from naturally infected water buffaloes (Bubalus bubalis) from Brazil. Veterinary Parasitology 124, 139150.CrossRefGoogle ScholarPubMed
Rozas, J., Sanchez-Del-Barrio, J. C., Messeguer, X. and Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 24962497.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. 2nd Edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.Google Scholar
Sharma, Y. D. (1992). Structure and possible function of heat-shock proteins of falciparum malaria. Comparative Biochemistry and Physiology 102B, 437444.Google Scholar
Sheppard, M., Kemp, D. J., Anders, R. F. and Lew, A. M. (1989). High level sequence homology between a Plasmodium chabaudi heat shock protein gene and its Plasmodium falciparum equivalent. Molecular and Biochemical Parasitology 37, 285288.Google Scholar
Siverajah, S., Ryce, C., Morrison, D. A. and Ellis, J. T. (2003). Characterization of an alpha tubulin gene sequence from Neospora caninum and Hammondia heydorni, and their comparison to homologous genes from Apicomplexa. Parasitology 126, 561569.Google ScholarPubMed
Šlapeta, J. and Keithly, J. S. (2004). Cryptosporidium parvum mitochondrial-type HSP70 targets homologous and heterologous mitochondria. Eukaryotic Cell 3, 483494.CrossRefGoogle ScholarPubMed
Šlapeta, J. R., Koudela, B., Votýpka, J., Modrý, D., Horejs, R. and Lukes, J. (2002 a). Coprodiagnosis of Hammondia heydorni in dogs by PCR based amplification of ITS-1 rRNA: differentiation from morphologically indistinguishable oocysts of Neospora caninum. Veterinary Journal 163, 147154.CrossRefGoogle ScholarPubMed
Šlapeta, J. R., Modrý, D., Kyselová, I., Horejs, R., Lukes, J. and Koudela, B. (2002 b). Dog shedding oocysts of Neospora caninum: PCR diagnosis and molecular phylogenetic approach. Veterinary Parasitology 109, 157167.CrossRefGoogle ScholarPubMed
Sreekumar, C., Hill, D. E., Miska, K. B., Rosenthal, B. M., Vianna, M. C. B., Venturini, L., Basso, W., Gennari, S. M., Lindsay, D. S. and Dubey, J. P. (2004). Hammondia heydorni: evidence of genetic diversity among isolates from dogs. Experimental Parasitology 107, 6571.CrossRefGoogle ScholarPubMed
Sulaiman, I. M., Morgan, U. M., Thompson, R. C., Lal, A. A. and Xiao, L. (2000). Phylogenetic relationships of Cryptosporidium parasites based on the 70-kilodalton heat shock protein (HSP70) gene. Applied and Environmental Microbiology 66, 23852391.CrossRefGoogle ScholarPubMed
Tamura, K. and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google ScholarPubMed
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.CrossRefGoogle Scholar
Xiao, L., Sulaiman, I. M., Ryan, U. M., Zhou, L., Atwill, E. R., Tischler, M. L., Zhang, X., Fayer, R. and Lal, A. A. (2002). Host adaptation and host–parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. International Journal for Parasitology 32, 17731785.CrossRefGoogle ScholarPubMed
Zhu, G., Keithly, J. S. and Philippe, H. (2000). What is the phylogenetic position of Cryptosporidium? International Journal of Systematic and Evolutionary Microbiology 50, 16731681.CrossRefGoogle ScholarPubMed