期刊论文详细信息
Particle and Fibre Toxicology
Sodalis glossinidius prevalence and trypanosome presence in tsetse from Luambe National Park, Zambia
Ewan T MacLeod1  Neil E Anderson2  Louise C Hamill2  Jemima E Horsley Downie1  Simon M Durkin1  Jonny W Dennis1 
[1] Division of Pathway Medicine, School of Biomedical Sciences, College of Medicine and Veterinary Medicine, The University of Edinburgh, Chancellor’s Building, 49 Little France Crescent, Edinburgh EH16 4SB, UK;The Royal (Dick) School of Veterinary Studies, University of Edinburgh, Roslin EH25 9RG, UK
关键词: Brevipalpis;    Pallidipes;    Morsitans;    Wildlife;    Rhodesiense;    Glossina;   
Others  :  1181858
DOI  :  10.1186/1756-3305-7-378
 received in 2014-06-26, accepted in 2014-08-01,  发布年份 2014
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【 摘 要 】

Background

Tsetse flies are the biological vectors of African trypanosomes, the causative agents of sleeping sickness in humans and nagana in animals. The tsetse endosymbiont Sodalis glossinidius has been suggested to play a role in tsetse susceptibility to infection. Here we investigate the prevalence of African trypanosomes within tsetse from the Luambe National Park, Zambia and if there is an association between S. glossinidius and presence of trypanosomes within the tsetse examined.

Methods

Tsetse representing three species (Glossina brevipalpis, Glossina morsitans morsitans and Glossina pallidipes), were sampled from Luambe National Park, Zambia. Following DNA extraction, PCR was used to examine the tsetse for presence of trypanosomes and the secondary endosymbiont S. glossinidius.

Results

S. glossinidius infection rates varied significantly between tsetse species, with G. brevipalpis (93.7%) showing the highest levels of infection followed by G. m. morsitans (17.5%) and G. pallidipes (1.4%). ITS-PCR detected a wide variety of trypanosomes within the tsetse that were analysed. Significant differences were found in terms of trypanosome presence between the three tsetse species. A high proportion of G. m. morsitans were shown to carry T. brucei s.l. DNA (73.7%) and of these around 50% were positive for Trypanosoma brucei rhodesiense. T. vivax, T. godfreyi, T. simiae, T. simiae Tsavo and T. congolense were also detected. No association was found between the occurrence of S. glossinidius and the presence of trypanosome DNA in any of the three tsetse species tested.

Conclusion

The current work shows that T. b. rhodesiense was circulating in Luambe National Park, representing a risk for people living in the park or surrounding area and for tourists visiting the park. The differences in trypanosome DNA presence observed between the different tsetse species tested may indicate host feeding preferences, as the PCR will not discriminate between a fly with an active/resident infection compared to a refractory fly that has fed on an infected animal. This makes it difficult to establish if S. glossinidius may play a role in the susceptibility of tsetse flies to trypanosome infection.

【 授权许可】

   
2014 Dennis et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Aksoy S: Tsetse–A haven for microorganisms. Parasitol Today 2000, 16:114-118.
  • [2]Akman L, Yamashita A, Watanabe H, Oshima K, Shiba T, Hattori M, Aksoy S: Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat Genet 2002, 32:402-407.
  • [3]Dale C, Maudlin I: Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int J Syst Bacteriol 1999, 49:267-275.
  • [4]Welburn SC, Arnold K, Maudlin I, Gooday GW: Rickettsia-like organisms and chitinase production in relation to transmission of trypanosomes by tsetse flies. Parasitology 1993, 107:141-145.
  • [5]Welburn SC, Maudlin I: Tsetse-trypanosome interactions: rites of passage. Parasitol Today 1999, 15:399-403.
  • [6]Hamidou Soumana I, Loriod B, Ravel S, Tchicaya B, Simo G, Rihet P, Geiger A: The transcriptional signatures of Sodalis glossinidius in the Glossina palpalis gambiensis flies negative for Trypanosoma brucei gambiense contrast with those of this symbiont in tsetse flies positive for the parasite: possible involvement of a Sodalis-hosted prophage in fly Trypanosoma refractoriness? Infect Genet Evol 2014, 24:41-56.
  • [7]Alam U, Medlock J, Brelsfoard C, Pais R, Lohs C, Balmand S, Carnogursky J, Heddi A, Takac P, Galvani A, Aksoy S: Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the tsetse fly Glossina morsitans. PLoS Pathog 2011, 7:e1002415.
  • [8]Lloyd L, Johnson WB: The trypanosome infections of tsetse flies in northern Nigeria and a new method of estimation. Bull Entomol Res 1924, 14:265-288.
  • [9]Okoth JO, Kapaata R: Trypanosome infection rates in Glossina fuscipes fuscipes Newst. in the Busoga sleeping sickness focus, Uganda. Ann Trop Med Parasitol 1986, 80:459-461.
  • [10]Masiga DK, McNamara JJ, Laveissière C, Truc P, Gibson WC: A high prevalence of mixed trypanosome infections in tsetse flies in Sinfra, Côte d’Ivoire, detected by DNA amplification. Parasitology 1996, 112:75-80.
  • [11]Auty HK, Picozzi K, Malele I, Torr SJ, Cleaveland S, Welburn S: Using molecular data for epidemiological inference: assessing the prevalence of Trypanosoma brucei rhodesiense in tsetse in Serengeti, Tanzania. PLoS Negl Trop Dis 2012, 6:e1501.
  • [12]Maudlin I: Inheritance of susceptibility to Trypanosoma congolense infection in Glossina morsitans. Ann Trop Med Parasitol 1982, 76:225-227.
  • [13]Hao Z, Kasumba I, Lehane MJ, Gibson WC, Kwon J, Aksoy S: Tsetse immune responses and trypanosome transmission: implications for the development of tsetse-based strategies to reduce trypanosomiasis. Proc Natl Acad Sci U S A 2001, 98:12648-12653.
  • [14]MacLeod ET, Maudlin I, Darby AC, Welburn SC: Antioxidants promote establishment of trypanosome infections in tsetse. Parasitology 2007, 134:827-831.
  • [15]Pais R, Lohs C, Wu Y, Wang J, Aksoy S: The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl Environ Microbiol 2008, 74:5965-5974.
  • [16]Maudlin I, Dukes P: Extrachromosomal inheritance of susceptibility to trypanosome infection in tsetse flies: I. selection of susceptible and refractory lines of Glossina morsitans morsitans. Ann Trop Med Parasitol 1985, 79:317-324.
  • [17]Moloo SK, Shaw MK: Rickettsial infections of midgut cells are not associated with susceptibility of Glossina morsitans centralis to Trypanosoma congolense infection. Acta Trop 1989, 46:223-227.
  • [18]Welburn SC, Gibson WC: Cloning of a repetitive DNA from the rickettsia-like organisms of tsetse flies (Glossina spp.). Parasitology 1989, 98:81-84.
  • [19]Maudlin I, Welburn SC, Mehlitz D: The relationship between rickettsia-like-organisms and trypanosome infections in natural populations of tsetse in Liberia. Trop Med Parasitol 1990, 41:265-267.
  • [20]O’Neill SL, Gooding RH, Aksoy S: Phylogenetically distant symbiotic microorganisms reside in Glossina midgut and ovary tissues. Med Vet Entomol 1990, 7:377-383.
  • [21]Geiger A, Ravel S, Frutos R, Cuny G: Sodalis glossinidius (Enterobacteriaceae) and vectorial competence of Glossina palpalis gambiensis and Glossina morsitans morsitans for Trypanosoma congolense savannah type. Curr Microbiol 2005, 51:35-40.
  • [22]Farikou O, Njiokou F, Mbida Mbida JA, Njitchouang GR, Djeunga HN, Asonganyi T, Simarro PP, Cuny G, Geiger A: Tripartite interactions between tsetse flies, Sodalis glossinidius and trypanosomes--an epidemiological approach in two historical human African trypanosomiasis foci in Cameroon. Infect Genet Evol 2010, 10:115-121.
  • [23]Wamwiri FN, Alam U, Thande PC, Aksoy E, Ngure RM, Aksoy S, Ouma JO, Murilla GA: Wolbachia, Sodalis and trypanosome co-infections in natural populations of Glossina austeni and Glossina pallidipes. Parasit Vectors 2013, 6:232. BioMed Central Full Text
  • [24]MacLeod ET: Factors Affecting Transmission of Trypanosomes Through Tsetse Flies. The University of Edinburgh, College of Medicine and Veterinary Medicine; 2005. [PhD Thesis]
  • [25]Baker RD, Maudlin I, Milligan PJ, Molyneux DH, Welburn SC: The possible role of Rickettsia-like organisms in trypanosomiasis epidemiology. Parasitology 1990, 100:209-217.
  • [26]Njiru ZK, Constantine CC, Guya S, Crowther J, Kiragu JM, Thompson RC, Dávila AM: The use of ITS1 rDNA PCR in detecting pathogenic African trypanosomes. Parasitol Res 2005, 95:186-192.
  • [27]Anderson NE: An Investigation into the Ecology of Trypanosomiasis in Wildlife of the Luangwa Valley, Zambia. University of Edinburgh, College of Medicine and Veterinary Medicine; 2009. [PhD thesis]
  • [28]Vale GA: Artificial refuges for tsetse flies (Glossina spp.). Bull Entomol Res 1971, 61:331-350.
  • [29]Chen X, Li S, Aksoy S: Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 1999, 48:49-58.
  • [30]Hamidou Soumana I, Berthier D, Tchicaya B, Thevenon S, Njiokou F, Cuny G, Geiger A: Population dynamics of Glossina palpalis gambiensis symbionts, Sodalis glossinidius, and Wigglesworthia glossinidia, throughout host-fly development. Infect Genet Evol 2013, 13:41-48.
  • [31]Matthew CZ: Biological and Molecular Aspects of Sodalis glossinidius. The University of Edinburgh, College of Medicine and Veterinary Medicine; 2007. [PhD Thesis]
  • [32]Picozzi K, Carrington M, Welburn SC: A multiplex PCR that discriminates between Trypanosoma brucei brucei and zoonotic T. b. rhodesiense. Exp Parasitol 2008, 118:41-46.
  • [33]Anderson NE, Mubanga J, Fevre EM, Picozzi K, Eisler MC, Thomas R, Welburn SC: Characterisation of the wildlife reservoir community for human and animal trypanosomiasis in the Luangwa Valley, Zambia. PLoS Negl Trop Dis 2011, 5:e1211.
  • [34]Lindh JM, Lehane MJ: The tsetse fly Glossina fuscipes fuscipes (Diptera: Glossina) harbours a surprising diversity of bacteria other than symbionts. Antonie Van Leeuwenhoek 2011, 99:711-720.
  • [35]Alam U, Hyseni C, Symula RE, Brelsfoard C, Wu Y, Kruglov O, Wang J, Echodu R, Alioni V, Okedi LM, Caccone A, Aksoy S: Implications of microfauna-host interactions for trypanosome transmission dynamics in Glossina fuscipes fuscipes in Uganda. Appl Environ Microbiol 2012, 78:4627-4637.
  • [36]Malele II, Magwisha HB, Nyingilili HS, Mamiro KA, Rukambile EJ, Daffa JW, Lyaruu EA, Kapange LA, Kasilagila GK, Lwitiko NK, Msami HM, Kimbita EN: Multiple trypanosoma infections are common amongst Glossina species in the new farming areas of Rufiji district, Tanzania. Parasit Vectors 2011, 4:217. BioMed Central Full Text
  • [37]Clausen PH, Adeyemi I, Bauer B, Breloeer M, Salchow F, Staak C: Host preferences of tsetse (Diptera: Glossinidae) based on bloodmeal identifications. Med Vet Entomol 1998, 12:169-180.
  • [38]Auty H, Anderson NE, Picozzi K, Lembo T, Mubanga J, Hoare R, Fyumagwa RD, Mable B, Hamill L, Cleaveland S, Welburn SC: Trypanosome diversity in wildlife species from the Serengeti and Luangwa Valley ecosystems. PLoS Negl Trop Dis 2012, 6:e1828.
  • [39]Malele II, Kinung’hi SM, Nyingilili HS, Matemba LE, Sahani JK, Mlengeya TD, Wambura M, Kibona SN: Glossina dynamics in and around the sleeping sickness endemic Serengeti ecosystem of northwestern Tanzania. J Vector Ecol 2007, 32:263-268.
  • [40]Lisulo M, Sugimoto C, Kajino K, Hayashida K, Mudenda M, Moonga L, Ndebe J, Nzala S, Namangala B: Determination of the prevalence of African trypanosome species in indigenous dogs of Mambwe district, eastern Zambia, by loop-mediated isothermal amplification. Parasit Vectors 2014, 7:19. BioMed Central Full Text
  • [41]Namangala B, Oparaocha E, Kajino K, Hayashida K, Moonga L, Inoue N, Suzuki Y, Sugimoto C: Preliminary investigation of trypanosomosis in exotic dog breeds from Zambia’s Luangwa and Zambezi valleys using LAMP. Am J Trop Med Hyg 2013, 89:116-118.
  • [42]Cottle LE, Peters JR, Hall A, Bailey JW, Noyes HA, Rimington JE, Beeching NJ, Squire SB, Beadsworth MB: Multiorgan dysfunction caused by travel-associated African trypanosomiasis. Emerg Infect Dis 2012, 18:287-289.
  • [43]Richter J, Göbels S, Göbel T, Westenfeld R, Müller-Stöver I, Häussinger D: A returning traveller with fever, facial swelling, and skin lesions. BMJ 2012, 344:e2092.
  • [44]Namangala B, Hachaambwa L, Kajino K, Mweene AS, Hayashida K, Simuunza M, Simukoko H, Choongo K, Chansa P, Lakhi S, Moonga L, Chota A, Ndebe J, Nsakashalo-Senkwe M, Chizema E, Kasonka L, Sugimoto C: The use of loop-mediated isothermal amplification (LAMP) to detect the re-emerging Human African trypanosomiasis (HAT) in the Luangwa and Zambezi valleys. Parasit Vectors 2012, 5:282. BioMed Central Full Text
  • [45]Welburn SC, Maudlin I: The nature of the teneral state in Glossina and its role in the acquisition of trypanosome infection in tsetse. Ann Trop Med Parasitol 1992, 86:529-536.
  • [46]Harley JM: Comparison of the susceptibility of infection with trypanosoma rhodesiense of Glossina pallidipes, G. morsitans, G. fuscipes and G. brevipalpis. Ann Trop Med Parasitol 1971, 55:185-189.
  • [47]Harley JM: The influence of the age of the fly at the time of the infecting feed on infection of Glossina fuscipes with Trypanosoma rhodesiense. Ann Trop Med Parasitol 1971, 65:191-196.
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