Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T10:27:55.690Z Has data issue: false hasContentIssue false
  • English
  • Français

Besnoitia neotomofelis n. sp. (Protozoa: Apicomplexa) from the southern plains woodrat (Neotoma micropus)

Published online by Cambridge University Press:  21 June 2010

J. P. DUBEY  and
M. J. YABSLEY
J. P. DUBEY*
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal and Natural Resources Institute, Animal Parasitic Diseases Laboratory, Building 1001, BARC-East, Beltsville, MD 20705-2350, USA
M. J. YABSLEY
Affiliation:
Warnell School of Forestry and Natural Resources and the Southeastern Cooperative Wildlife Disease Study, Department of Population Health, College of Veterinary Medicine, University of Georgia, Athens, GA30602, USA
*
*Corresponding author: USDA, ARS, ANRI, APDL, BARC-East, Building 1001, Beltsville, MD 20705, USA. Tel: +1 301 504 8128. Fax: +1301 504 9222. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Certain species of the protozoan genus Besnoitia cause clinical disease in livestock and wildlife. In the present paper a new species, Besnoitia neotomofelis is described from the southern planes woodrat (Neotoma micropus). The parasite was detected by bioassay of woodrat tissues in outbred Swiss Webster mice in an attempt to isolate Toxoplasma gondii. Initially, the organism was misdiagnosed as T. gondii because it was highly pathogenic for mice and its tachyzoites resembled T. gondii tachyzoites. Further studies revealed that it differed structurally and biologically from T. gondii. Tachyzoites were successfully cultivated and maintained in vitro in bovine monocytes and African green monkey kidney cells, and in vivo in mice. Non-dividing, uninucleate tachyzoites were approximately 1×5 μm in size. Longitudinally-cut bradyzoites in tissue sections measured 1·5–1·6×7·7–9·3 μm. Tissue cysts were microscopic, up to 210 μm long, and were infective orally to mice. Cats fed tissue cysts shed unsporulated 13×14 μm sized oocysts. All mice inoculated with B. neotomofelis died of acute besnoitiosis, irrespective of the dose, and Norwegian rats became infected but remained asymptomatic. Entero-epithelial stages (schizonts, gamonts) were found in cats fed tissue cysts. Large (up to 40×50 μm) first-generation schizonts developed in the lamina propria of the small intestine of cats. A second generation of small sized (8 μm) schizonts containing 4–8 merozoites was detected in enterocytes of the small intestine. Gamonts and oocysts were seen in goblet cells of the small intestinal epithelium. Tachyzoites were present in mesenteric lymph nodes of cats. Phylogenetic analysis indicated that B. neotomofelis was related to other Besnoitia species from rodents, rabbits, and opossums. Besnoitia neotomofelis is distinct from the 3 other species of Besnoitia, B. wallacei, B. darlingi and B. oryctofelisi that utilize cats as a definitive host.

Keywords

Besnoitia neotomofelis n. sp.woodratcatsmiceschizontscell cultureUSA
Type
Research Article
Information
Parasitology , Volume 137 , Issue 12 , October 2010 , pp. 1731 - 1747
Creative Commons
This is a work of the U.S. Government and is not subject to copyright protection in the United States.
Copyright
Copyright © Cambridge University Press 2010. This is a work of the U.S. Government and is not subject to copyright protection in the United States.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bostrom, B., Wolf, C., Greene, C. and Peterson, D. S. (2008). Sequence conservation in the rRNA first internal transcribed spacer region of Babesia gibsoni genotype Asia isolates. Veterinary Parasitology 152, 152–157.CrossRefGoogle ScholarPubMed
Chinchilla, M. and Frenkel, J. K. (1978). Mediation of immunity to intracellular infection (Toxoplasma and Besnoitia) within somatic cells. Infection and Immunity 19, 999–1012.CrossRefGoogle ScholarPubMed
Cortes, H. C. E., Reis, Y., Waap, H., Vidal, R., Soares, H., Marques, I., Pereira da Fonseca, I., Fazendeiro, I., Ferreira, M. L., Caeiro, V., Shkap, V., Hemphill, A. and Leitão, A. (2006). Isolation of Besnoitia besnoiti from infected cattle in Portugal. Veterinary Parasitology 141, 226–233.CrossRefGoogle ScholarPubMed
Dubey, J. P. (1995). Duration of immunity to shedding of Toxoplasma gondii oocyst by cats. Journal of Parasitology 81, 410–415.CrossRefGoogle ScholarPubMed
Dubey, J. P. (2009). Toxoplasmosis of Animals and Humans. 2nd Edn. CRC Press, Boca Raton, Florida, USA.Google Scholar
Dubey, J. P. and Desmonts, G. (1987). Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19, 336–339.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Frenkel, J. K. (1976). Feline toxoplasmosis from acutely infected mice and the development of Toxoplasma cysts. Journal of Protozoology 23, 537–546.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Lindsay, D. S. (1998). Isolation in immunodeficient mice of Sarcocystis neurona from opossum (Didelphis virginiana) faeces, and its differentiation from Sarcocystis falcatula. International Journal for Parasitology 28, 1823–1828.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Lindsay, D. S. (2003). Development and ultrastructure of Besnoitia oryctofelisi tachyzoites, tissue cysts, bradyzoites, schizonts and merozoites. International Journal for Parasitology 33, 807–819.CrossRefGoogle ScholarPubMed
Dubey, J. P., Lindsay, D. S. and Speer, C. A. (1998). Structure of Toxoplasma gondii tachyzoites, bradyzoites and sporozoites, and biology and development of tissue cysts. Clinical Microbiology Reviews 11, 267–299.CrossRefGoogle ScholarPubMed
Dubey, J. P., Lindsay, D. S., Rosenthal, B. M., Sreekumar, C., Hill, D. E., Shen, S. K., Kwok, O. C. H., Rickard, L. G., Black, S. S. and Rashmir-Raven, A. (2002). Establishment of Besnoitia darlingi from opossums (Didelphis virginiana) in experimental intermediate and definitive hosts, propagation in cell culture, and description of ultrastructural and genetic characteristics. International Journal for Parasitology 32, 1053–1064.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Sreekumar, C. (2003). Redescription of Hammondia hammondi and its differentiation from Toxoplasma gondii. International Journal for Parasitology 33, 1437–1453.CrossRefGoogle ScholarPubMed
Dubey, J. P., Sreekumar, C., Lindsay, D. S., Hill, D., Rosenthal, B. M., Venturini, L., Venturini, M. C. and Greiner, E. C. (2003 a). Besnoitia oryctofelisi n. sp. (Protozoa: Apicomplexa) from domestic rabbits. Parasitology 126, 521–539.Google Scholar
Dubey, J. P., Sreekumar, C., Rosenthal, B. M., Lindsay, D. S., Grisard, E. C. and Vitor, R. W. A. (2003 b). Biological and molecular characterization of Besnoitia akodoni n. sp. (Protozoa: Apicomplexa) from the rodent Akodon montensis in Brazil. Parassitologia 45, 61–70.Google Scholar
El Sheikha, H. M., Hussein, H. S., Monib Mel, S. and Mansfield, L. S. (2007). Observations on besnoitiosis in Virginia opossum (Didelphis virginiana) from Michigan, USA. Journal of the Egyptian Society of Parasitology 37, 1–16.Google ScholarPubMed
Fernández-García, A., Risco-Castillo, V., Pedraza-Díaz, S., Aguado-Martínez, A., Álvarez-García, G. and Gómez-Bautista, M. (2009). First isolation of Besnoitia besnoiti from a chronically infected cow in Spain. Journal of Parasitology 95, 474–476.CrossRefGoogle ScholarPubMed
Frenkel, J. K. (1953). Infections with organisms resembling Toxoplasma, together with the description of a new organism: Besnoitia jellisoni. Atti del VI Congresso Internazionale di Microbiologia 5, 426–434.Google Scholar
Frenkel, J. K. (1956). Effects of hormones on the adrenal necrosis produced by Besnoitia jellisoni in golden hamsters. Journal of Experimental Medicine 103, 375–398.CrossRefGoogle ScholarPubMed
Frenkel, J. K. (1977). Besnoitia wallacei of cats and rodents: with a reclassification of other cyst-forming isosporoid coccidia. Journal of Parasitology 63, 611–628.CrossRefGoogle ScholarPubMed
Frenkel, J. K. and Lunde, M. N. (1966). Effects of corticosteroids on antibody and immunity in Besnoitia infection of hamsters. Journal of Infectious Diseases 116, 414–424.CrossRefGoogle ScholarPubMed
Frenkel, J. K. and Wilson, H. R. (1972). Effects of radiation on specific cellular immunities: besnoitiosis and a herpesvirus infection of hamsters. Journal of Infectious Diseases 125, 216–230.CrossRefGoogle Scholar
Kumar, S., Tamura, K. and Nei, M. (2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.CrossRefGoogle ScholarPubMed
Leighton, F. A. and Gajadhar, A. A. (2001). Besnoitia spp. and besnoitiosis. In Parasitic Diseases of Wild Mammals (ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 468–478. Iowa State University Press, Ames, IO, USA.CrossRefGoogle Scholar
Lunde, M. N. and Jacobs, L. (1965). Antigenic relationship of Toxoplasma gondii and Besnoitia jellisoni. Journal of Parasitology 51, 273–276.CrossRefGoogle ScholarPubMed
McAllister, M. M., Parmley, S. F., Weiss, L. M., Welch, V. J. and McGuire, A. M. (1996). An immunohistochemical method for detecting bradyzoite antigen (BAG5) in Toxoplasma gondii-infected tissues cross-reacts with a Neospora caninum bradyzoite antigen. Journal of Parasitology 82, 354–355.CrossRefGoogle ScholarPubMed
Mehlhorn, H., Klimpel, S. and Schein, E. (2009). Another African disease in Central Europa: besnoitiosis of cattle. I. Light and electron microscopical study. Parasitology Research 104, 861–868.CrossRefGoogle ScholarPubMed
Schares, G., Basso, W., Majzoub, M., Cortes, H. C. E., Rostaher, A., Selmair, J., Hermanns, W., Conraths, F. J. and Gollnick, N. S. (2009). First in vitro isolation of Besnoitia besnoiti from chronically infected cattle in Germany. Veterinary Parasitology 163, 315–322.CrossRefGoogle ScholarPubMed
Smith, D. D. and Frenkel, J. K. (1977). Besnoitia darlingi (Protozoa: Toxoplasmatinae): cyclic transmission by cats. Journal of Parasitology 63, 1066–1071.CrossRefGoogle ScholarPubMed
Wallace, G. D. and Frenkel, J. K. (1975). Besnoitia species (Protozoa, Sporozoa, Toxoplasmatidae): recognition of cyclic transmission by cats. Science 188, 369–371.CrossRefGoogle ScholarPubMed
Yabsley, M. J., Work, T. M. and Rameyer, R. A. (2006). Molecular phylogeny of Babesia poelea from brown boobies (Sula leucogaster) from Johnston Atoll, Central Pacific. Journal of Parasitology 92, 423–425.CrossRefGoogle ScholarPubMed