Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-27T22:09:30.001Z Has data issue: false hasContentIssue false
  • English
  • Français

Trypanosoma (Nannomonas) godfreyi sp. nov. from tsetse flies in The Gambia: biological and biochemical characterization

Published online by Cambridge University Press:  06 April 2009

J. J. McNamara ,
G. Mohammed  and
W. C. Gibson
J. J. McNamara
Affiliation:
MRC Trypanosomiasis Research Group, University of Bristol, Churchill Building, Langford, Bristol BS18 7DY, UK
G. Mohammed
Affiliation:
Department of Veterinary Surgery and Medicine, Faculty of Veterinary Medicine, Ahmadu Bello University, Samaru, Zaria, Nigeria Department of Pathology and Microbiology, University of Bristol, Churchill Building, Langford, Bristol BS18 7DY, UK
W. C. Gibson
Affiliation:
Department of Pathology and Microbiology, University of Bristol, Churchill Building, Langford, Bristol BS18 7DY, UK
Get access Rights & Permissions [Opens in a new window]

Summary

We provide evidence from isoenzyme analysis, hybridization with repetitive DNA probes, behavioural studies and morphometrics that 4 trypanosome isolates from Glossina morsitans submorsitans in The Gambia constitute a new species now named Trypanosoma (Nannomonas) godfreyi. The bloodstream trypomastigotes of T. (N.) godfreyi are relatively small with a mean length of 13·7 μm (range: 9·1–21·8 μm) and a mean width of 1·65 μm (range: 0·65–2·69 μm). There is no free flagellum and the marginal kinetoplast is subterminal to a rounded posterior end; the undulating membrane is usually conspicuous. As with other Nannomonas, T. godfreyi developed in the midgut and proboscis of Glossina and infections matured in 21–28 days in laboratory G. m. morsitans. In The Gambia the normal vertebrate host appears to be the warthog, Phacochoerus aethiopicus, although elsewhere other wild and domestic suids may also be implicated in the life-cycle. T. godfreyi was identified unequivocally using a 380 bp DNA probe specific for a major genomic repeat sequence; its isoenzyme profile distinguished it clearly from T. simiae and three strain groups of T. congolense: savannah, riverine-forest and kilifi.

Keywords

trypanosomeNannomonasTrypanosoma godfreyiporcine trypanosomiasis
Type
Research Article
Information
Parasitology , Volume 109 , Issue 4 , November 1994 , pp. 497 - 509
Copyright
Copyright © Cambridge University Press 1994

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

Agu, W. E. (1984). Comparative study of the susceptibility to infection with Trypanosoma simiae of Glossina morsitans and G. tachinoides. Acta Tropica 41, 131–4.Google ScholarPubMed
Browning, C. H. (1908). Chemotherapy in trypanosome infections: an experimental study. Journal of Pathology and Bacteriology 12, 166–90.CrossRefGoogle Scholar
Chardome, M. & Peel, E. (1954). Etude experimentale d'une souche appelée T. congolense var. berghei transmise par Glossina brevipalpis du Mosso (Urundi). Annales de la Société belge de Médecine Tropicale 34, 311–20.Google ScholarPubMed
Chardome, M. & Peel, E. (1967). Les Trypansomes Transmis par Glossina morsitans au Bugesera (Rwanda et Burundi). Brussels: Goemaere.Google Scholar
Cibulskis, R. (1984). Mutation and recombination in the Trypanosomatidae. In Leishmania. Taxonomie et Phylogenèse, pp. 297–303. IMEE, Montpellier.Google Scholar
Cunningham, I. (1977). New culture medium for the maintenance of tsetse tissues and growth of trypanosomatids. Journal of Protozoology 24, 325–9.CrossRefGoogle ScholarPubMed
Desowitz, R. S. & Watson, H. J. C. (1953). The maintenance of a strain of Trypanosoma simiae in rabbits. Annals of Tropical Medicine and Parasitology 47, 324–34.CrossRefGoogle ScholarPubMed
Dickin, S. K. & Gibson, W. C. (1989). Hybridisation with a repetitive DNA probe reveals the presence of small chromosomes in Trypanosoma vivax. Molecular and Biochemical Parasitology 33, 135–42.CrossRefGoogle ScholarPubMed
Dukes, P., Faye, J., McNamara, J. J., Snow, W. F., Rawlings, P., Dwinger, R. H. & Brun, R. (1989). Isolation and cultivation in vitro to the infective, metacyclic stage of Trypanosoma (Nannomonas) simiae from Glossina morsitans submorsitans. Acta Tropica 46, 191–203.CrossRefGoogle Scholar
Dukes, P., McNamara, J. J. & Godfrey, D. G. (1991). Elusive trypanosomes. Annals of Tropical Medicine and Parasitology 85, 21–32.CrossRefGoogle ScholarPubMed
Dunn, G. & Everitt, B. S. (1982). Cluster analysis. In An Introduction to Mathematical Taxonomy, pp. 77–105. Cambridge: Cambridge University Press.Google Scholar
Feinberg, A. P. & Vogelstein, B. (1983). A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Annals of Biochemistry 132, 6–13.CrossRefGoogle ScholarPubMed
Garside, L., Bailey, M. & Gibson, W. (1994). DNA content and molecular karyotype of trypanosomes of the subgenus Nannomonas. Acta Tropica (in the Press.)CrossRefGoogle ScholarPubMed
Gashumba, J. K. (1990). Speciation and subspeciation in Nannomonas trypanosomes and their epidemiological significance. Insect Science and Application 11, 265–9.Google Scholar
Gashumba, J. K., Baker, R. D. & Godfrey, D. G. (1988). Trypanosoma congolense: The distribution of enzymic variants in East and West Africa. Parasitology 96, 475–86.CrossRefGoogle ScholarPubMed
Gashumba, J. K., Gibson, W. C. & Opiyo, E. A. (1986). A preliminary comparison of Trypanosoma simiae and T. congolense by isoenzyme electrophoresis. Acta Tropica 43, 15–19.Google Scholar
Gibson, W. C., Dukes, P. & Gashumba, J. K. (1988). Species-specific DNA probes for the identification of African trypanosomes in tsetse flies. Parasitology 96, 1–12.Google Scholar
Gibson, W. C., Marshall, T. F.De, C. & Godfrey, D. G. (1980). Numerical analysis of enzyme polymorphism: new approach to the epidemiology and taxonomy of trypanosomes of the subgenus Trypanozoon. Advances in Parasitology 18, 175–246.CrossRefGoogle Scholar
Gibson, W. C., Mehlitz, D., Lanham, S. M. & Godfrey, D. G. (1978). The identification of Trypanosoma brucei gambiense in Liberian pigs and dogs by isoenzymes and by resistance to human plasma. Tropenmedizin und Parasitologie 29, 335–45.Google ScholarPubMed
Godfrey, D. G. (1960). Types of Trypanosoma congolense. I. Morphological differences. Annals of Tropical Medicine and Parasitology 54, 428–38.CrossRefGoogle ScholarPubMed
Godfrey, D. G. (1961). Types of Trypanosoma congolense. II. Differences in the courses of infection. Annals of Tropical Medicine and Parasitology 55, 154–66.CrossRefGoogle ScholarPubMed
Godfrey, D. G. (1977). Problems in distinguishing between the morphologically similar trypanosomes of mammals. Protozoology 3, 33–49.Google Scholar
Godfrey, D. G. (1982). Diversity within T. congolense. In Perspectives in Trypanosomiasis Research (ed. Baker, J. R.), pp. 37–46. Chichester: Research Studies Press.Google Scholar
Godfrey, D. G. (1984). Molecular biochemical characterisation of human parasites. Recent Advances in Tropical Medicine 1, 289–319.Google Scholar
Gray, M. A., Hirumi, H. & Gardiner, P. R. (1987). Salivarian trypanosomes (insect forms). In In Vitro Methods for Parasite Cultivation (ed. Taylor, A. E. R. & Baker, J. R.), pp. 118–52. London: Academic Press.Google Scholar
Gray, M. A., Ross, C. A., Taylor, A. M. & Luckins, A. G. (1984). In vitro cultivation of Trypanosoma congolense: the production of infective metacyclic trypanosomes in cultures initiated from cloned stocks. Acta Tropica 41, 343–53.Google ScholarPubMed
Herbert, W. J. & Lumsden, W. H. R. (1976). Trypanosoma brucei: A rapid ‘matching’ method for estimating the host's parasitaemia. Experimental Parasitology 40, 427–31.CrossRefGoogle Scholar
Hoare, C. A. (1972). The Trypanosomes of Mammals. A Zoological Monograph. Oxford: Blackwell Scientific Publications.Google Scholar
Huxley, J. (1963). Evolution, the Modern Synthesis, 2nd edn.London: Allen and Unwin.Google Scholar
Ilemobade, A. A. & Balogun, T. F. (1981). Pig trypanosomiasis: effects of infection on feed intake, live weight gain and carcass traits. Tropical Animal Health and Production 13, 128–36.CrossRefGoogle Scholar
Jaccard, P. (1908). Nouvelles recherches sur la distribution florale. Bulletin Société Vaudoise Science Nat. 44, 223–70.Google Scholar
Janssen, J. A. H. A. & Wijers, D. J. B. (1974). Trypanosoma simiae at the Kenya coast. A correlation between virulence and the transmitting species of Glossina. Annals of Tropical Medicine and Parasitology 68, 5–19.CrossRefGoogle Scholar
Jenni, L., Marti, S., Schweizer, J., Betschart, B., le Page, R. W. F., Wells, J. M., Tait, A., Paindavoine, P., Pays, E. & Steinert, M. (1986). Hybrid formation between African trypanosomes during cyclical transmission. Nature, London 322, 173–5.CrossRefGoogle ScholarPubMed
Johnson, P. J. & Borst, P. (1986). Mapping of VSG genes on large expression site chromosomes of Trypanosoma brucei separated by pulsed-field gradient electrophoresis. Gene 43, 213–20.CrossRefGoogle ScholarPubMed
Jordan, A. M. (1964). Trypanosome infection rates in Glossina morsitans submorsitans Newst. in Nothern Nigeria. Bulletin of Entomological Research 55, 219–31.CrossRefGoogle Scholar
Kaukas, A., Gashumba, J. K., Lanham, S. M. & Dukes, P. (1990). The substitution of procyclic for bloodstream form Trypanosoma brucei gambiense in isoenzyme studies. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 242–5.CrossRefGoogle ScholarPubMed
Killick-Kendrick, R. & Godfrey, D. G. (1963). Observations on a close association between Glossina tachinoides and domestic pigs near Nsukka, eastern Nigeria. I. Trypanosoma congolense and T. brucei infections in the pigs. Annals of Tropical Medicine and Parasitology 57, 225–31.CrossRefGoogle Scholar
Knowles, G., Betschart, B., Kukla, B. A., Scott, J. R. & Majiwa, P. A. O. (1988). Genetically discrete populations of Trypanosoma congolense from livestock on the Kenyan coast. Parasitology 96, 461–74.CrossRefGoogle ScholarPubMed
Kukla, B. A., Majiwa, P. A. O., Young, J. R., Moloo, S. K. & Ole-Moiyoi, O. (1987). Use of species-specific DNA probes for detection and identification of trypanosome infection in tsetse flies. Parasitology 95, 1–26.CrossRefGoogle ScholarPubMed
Lanham, S. M., Grendon, J. M., Miles, M. A., Povoa, M. M. & Almeida De Souza, A. A. (1981). A comparison of electrophoretic methods for isoenzyme characterization of trypanosomatids. I. Standard stocks of Trypanosoma cruzi zymodemes from northeast Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 742–50.CrossRefGoogle ScholarPubMed
le Blancq, S. M., Schnur, L. F. & Peters, W. (1986). Leishmania in the Old World. 1. The geographical and hostal distribution of L. major zymodemes. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 99–122.CrossRefGoogle ScholarPubMed
Lumsden, W. H. R. & Ketteridge, D. S. (1979). Characterization, nomenclature and maintenance of salivarian trypanosomes. In Biology of the Kinetoplastida, vol. 2, pp. 693–721. London: Academic Press.Google Scholar
Mackenzie, P. K. I. & Boyt, W. P. (1969). Notes upon a trypanosome strain resembling T. congolense apparently completely adapted to the porcine species. British Veterinary Journal 125, 414–21.CrossRefGoogle Scholar
Majiwa, P. A. O., Maina, M., Waitumbi, J. N., Mihok, S. & Zweygarth, E. (1993). Trypanosoma (Nannomonas) congolense: molecular characterization of a new genotype from Tsavo, Kenya. Parasitology 106, 151–62.CrossRefGoogle ScholarPubMed
Majiwa, P. A. O. & Webster, P. (1987). A repetitive deoxyribonucleic acid sequence distinguishes Trypanosoma simiae from T. congolense. Parasitology 95, 543–98.CrossRefGoogle ScholarPubMed
Maudlin, I. & Dukes, P. (1985). Extrachromosomal inheritance of susceptibility to trypanosome infection in tsetse flies. I. Selection of susceptible and refractory lines of Glossina morsitans morsitans. Annals of Tropical Medicine and Parasitology 79, 317–24.CrossRefGoogle ScholarPubMed
McNamara, J., Dukes, P., Snow, W. F. & Gibson, W. C. (1989). Use of DNA probes to identify Trypanosoma congolense and T. simiae in tsetse flies from The Gambia. Acta Tropica 46, 55–61.CrossRefGoogle Scholar
McNamara, J. J. & Snow, W. F. (1991). Improved identification of Nannomonas infections in tsetse flies from The Gambia. Acta Tropica 48, 127–36.CrossRefGoogle Scholar
Mews, A. R., Langley, P. A., Pimley, R. W. & Flood, M. E. T. (1977). Large-scale rearing of tsetse flies (Glossina spp.) in the absence of a living host. Bulletin of Entomological Research 67, 119–28.CrossRefGoogle Scholar
Mohammed, G. (1991). The comparative pathogenicities of genetically defined trypanosomes of the subgenus Nannomonas with special reference to a new species. Ph.D. thesis, University of Bristol.Google Scholar
Moore, B., Nierenstein, M. & Todd, J. L. (1908). Notes on the effects of therapeutic agents on trypanosomes in respect to (a) acquired resistance of the parasite to the drug; and (b) changes in virulence of the strains after escape from the drug. Annals of Tropical Medicine and Parasitology 2, 221–6.CrossRefGoogle Scholar
Murray, M., Murray, P. K. & McIntyre, W. I. M. (1977). An improved parasitological technique for the diagnosis of African trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 325–6.CrossRefGoogle ScholarPubMed
Nantulya, V. M., Doyle, J. J. & Jenni, L. (1978). Studies on Trypanosoma (Nannomonas) congolense. 2. Observations on the cyclical transmission of three field isolates by Glossina morsitans morsitans. Acta Tropica 35, 339–44.Google Scholar
Opiyo, E. A. (1984). Studies on the biology of Trypanosoma (Nannomonas) simiae. Ph.D. thesis, University of Nairobi.Google Scholar
Opiyo, E. A., Kinoti, G. K. & Otieno, L. H. (1988). Adaptation of the pig parasite Trypanosoma simiae to the laboratory rat. Annals of Tropical Medicine and Parasitology 82, 397–8.CrossRefGoogle Scholar
Peel, E. & Chardome, M. (1954 a). Etude experimentale de souches de Trypanosoma simiae Bruce 1912, transmises par Glossina brevipalpis du Mosso (Urundi). Annales de la Société belge de Médecine Tropicale 34, 345–59.Google ScholarPubMed
Peel, E. & Chardome, M. (1954 b). Etude experimentale d'une souche appelée Trypanosoma congolense var. urundiense transmise par Glossina brevipalpis Newst., du Mosso (Urundi). Annales de la Société belge de Médecine Tropicale 34, 303–10.Google Scholar
Rawlings, P., Dwinger, R. H. & Snow, W. F. (1991). An analysis of survey measurement of tsetse challenge to trypanotolerant cattle in relation to aspects of analytical models of trypanosomiasis. Parasitology 102, 371–7.CrossRefGoogle ScholarPubMed
Roberts, C. J. (1971). The lack of infectivity to cattle of a strain of Trypanosoma simiae transmitted by Glossina morsitans and G. tachinoides. Annals of Tropical Medicine and Parasitology 65, 319–26.CrossRefGoogle ScholarPubMed
Ross, C. A., Gray, M. A., Taylor, A. M. & Luckins, A. G. (1985). In vitro cultivation of T. congolense: establishment of infective mammalian forms in continuous culture after isolation from the blood of infected mice. Acta Tropica 42, 113–22.Google ScholarPubMed
Schwartz, D. C. & Cantor, C. R. (1984). Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell 37, 67–75.CrossRefGoogle ScholarPubMed
Sloof, P., Bos, J. L., Konings, A. F. J. M., Menke, H. H., Borst, P., Gutteridge, W. E. & Leon, W. (1983). Characterization of satellite DNA in Trypanosoma brucei and T. cruzi. Journal of Molecular Biology 167, 1–21.CrossRefGoogle Scholar
Southern, E. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. Journal of Molecular Biology 98, 503–17.CrossRefGoogle ScholarPubMed
Stephen, L. E. (1962). Some observations on the behaviour of trypanosomes occurring in cattle previously treated with prophylactic drugs. Annals of Tropical Medicine and Parasitology 56, 415–21.CrossRefGoogle Scholar
Stephen, L. E. (1966). Pig Trypanosomiasis in Africa. Review series No. 8. Farnham Royal: Commonwealth Agricultural Bureaux.Google Scholar
Stephen, L. E. (1986). Trypanosomiasis. A Veterinary Perspective. Oxford: Pergamon Press.Google Scholar
Stevens, J. R. & Cibulskis, R. (1990). Analysing isoenzyme band patterns using similarity coefficients: a PC program. Computer Methods and Programs in Biomedicine 33, 205–12.CrossRefGoogle Scholar
Stevens, J. R., Nunes, V. L. B., Lanham, S. M. & Oshiro, E. T. (1989). Isoenzyme characterization of Trypanosoma evansi isolated from capybaras and dogs in Brazil. Acta Tropica 46, 213–22.CrossRefGoogle ScholarPubMed
Stewart, J. L. (1947). Porcine trypanosomiasis. Veterinary Record 59, 648.Google ScholarPubMed
Tibayrenc, M. (1993). Entamoeba, Giardia, and Toxoplasma: clones or cryptic species? Parasitology Today 9, 102–5.CrossRefGoogle ScholarPubMed
Van Der Ploeg, L. H. T., Bernards, A., Rijsewijk, F. & Borst, P. (1982). Characterization of the DNA duplication-transposition that controls the expression of two genes for the variant surface glycoproteins in Trypanosoma brucei. Nucleic Acids Research 10, 593–609.CrossRefGoogle ScholarPubMed
Van Der Ploeg, L. T. H., Schwartz, D. C., Cantor, C. R. & Borst, P. (1984). Antigenic variation in Trypanosoma brucei analysed by electrophoretic separation of chromosome sized DNA molecules. Cell 37, 77–84.CrossRefGoogle Scholar
Van Dijk, J., Zwart, D. & Leeflang, P. (1973). A contribution to the pathology of T. simiae infection in pigs. Zentralblatt für Veterinärmedizin, B 20, 374.CrossRefGoogle Scholar
Wilson, A. J. (1969). Value of indirect fluorescent antibody test as a serological aid to diagnosis of Glossina transmitted bovine trypanosomiasis. Tropical Animal Health and Production 1, 89–95.CrossRefGoogle Scholar
World Health Organization (1986). Epidemiology and control of African trypanosomiasis. WHO Technical Report Series No. 739. Geneva: World Health Organization.Google Scholar
Woolhouse, M. E. J., Hargrove, J. W. & McNamara, J. J. (1993). Epidemiology of trypanosome infections of the tsetse fly Glossina pallidipes in the Zambezi valley. Parasitology 106, 479–85.CrossRefGoogle ScholarPubMed
Young, C. J. (1980). Zymodemes of Trypanosoma congolense and a preliminary assessment of their epidemiological significance. Ph.D. thesis, University of London.Google Scholar
Young, C. J. & Godfrey, D. G. (1983). Enzyme polymorphism and the distribution of Trypanosoma congolense isolates. Annals of Tropical Medicine and Parasitology 77, 467–81.CrossRefGoogle ScholarPubMed
Zweygarth, E., Rottcher, D. & Schillinger, D. (1987). Failure of Trypanosoma (Nannomonas) simiae to infect camels (Camelus dromedarius). Acta Tropica 44, 97–8.Google ScholarPubMed