Improving SIT for Tsetse Flies through Research on their Symbionts and Pathogens
Closed for Proposals
Project Type
Coordinated Research ProjectProject Code
D42012
CRP
1375
Approved Date
29 April 2006Project Status
ClosedStart Date
15 March 2007Expected End Date
31 March 2012Completed Date
26 April 2012Description
The successful eradication of the tsetse population on the island of Zanzibar using the SIT has encouraged Member States to request the expansion of this technology to the African mainland as part of efforts to establish tsetse-free areas in key regions of sub-Saharan Africa. This goal has now also been endorsed by the Member States of the African Union. Area-wide programmes with a SIT component are currently in preparation in a number of countries in western, eastern and southern Africa. Microbial associations, beneficial and pathogenic in nature, can influence the efficiency and implementation of area-wide integrated pest management programmes that integrate the SIT. These microbes provide novel opportunities to enhance the SIT applications in the field, while they can also present problems for establishing the large healthy colonies needed to apply this technology to tsetse. A new CRP, harnessing the recent developments in tsetse, symbiont and pathogen genetics and genomics, has the potential to improve upon the efficiency and efficacy of SIT applications on the mainland. The new CRP will focus on the development of methods to manage the virus infection in tsetse colonies, an assessment of natural incompatibility related to the presence of Wolbachia, the development of improved population suppression methods using fungal pathogens and the development of tsetse strains refractory to infection by trypanosomes
Objectives
The overall objective of the CRP was to understand and exploit interactions between tsetse flies and their microbes to enhance the efficacy of tsetse SIT programmes.
Specific Objectives of the CRP:
To clarify tsetse, symbiont and other microbe interactions
To better understand and manage tsetse - virus interactions in laboratory populations
To manipulate microbial flora to express parasite refractoriness traits
To harness symbiont mediated natural mating incompatibilities
To improve tsetse suppression technologies
To disseminate knowledge among disease endemic country researchers to improve field application of SIT through better decision making and capacity building.
Specific Objectives
1-Decipher host-symbiont interactions to understand tsetse’s nutritional ecology and improve mass rearing procedures,
10-Disseminate discoveries to endemic countries and interested parties and relevant databases
11-Harness cytoplasmic incompatibility for SIT application
11-Publish results in scientific journals
2-Investigate tsetse pathogen interactions to improve tsetse control
3- Study the population dynamics of tsetse microbial flora
4-To understand and manage tsetse virus interactions in laboratory populations
a. identify DNA database for virus populations
b. determine transmission mode of tsetse SGHV
c. maintain SGH symptom free colonies
5-Develop parasite refractory lines,
6-Identify trypanosome inhibitory products
7-Incorporate parasite resistance traits into SIT lines
8-Cytoplasmic incompatibility-mediated gene drive system
Impact
The CRP has resulted in some important achievement which will help in improving the tsetse mass production for SIT program. These achievements include the following:
1-Decipher host-symbiont interactions to understand tsetse’s nutritional ecology and improve mass rearing procedures:
i- Developed the methodology to generate fertile tsetse lines without symbionts through dietary supplementation,
ii- Obtained Knowledge on the functional role of Wigglesworthia in tsetse symbiosis.
2-Investigate tsetse pathogen interactions to improve tsetse control:
see 4 below.
3-Study the population dynamics of tsetse microbial flora:
i- Discovered varying Sodalis genotypes in natural populations,
ii- Observed correlation of Sodalis occurrence with parasite infection in natural populations.
4-To understand and manage tsetse virus interactions in laboratory populations
a. DNA database for virus populations identified:
i- identified and characterized the causal agent (SGHV) of salivary gland hypertrophy,
ii- sequenced, annotated, and published genomes of three SGHVs (two strains of GpSGHV and one strain of MdSGHV),
iii- classified a novel virus family (Hytrosaviridae) with two genera (Glossinavirus and Muscavirus), accepted by the ICTV; proposed that hytroviruses are related phylogenetically with baculoviruses and nudiviruses,
iv- genomic sequence provided a framework to:
- developed specific and universal PCR primers to detect virus in field and laboratory tsetse colonies,
- identified genes that are stable, essential, and suitable candidates for the development of antiviral therapies,
- identified antiviral dsRNAs for RNAi suppression of viral replication,
- evaluated the level of GpSGHV genetic diversity in field and laboratory tsetse fly populations,
- determined the SGHV proteomes and identified targets for the development of antibodies to suppress viral infection.
b. Transmission mode of tsetse SGHV determined:
i- recognized that in field populations the primary mode of transmission is vertical whereas in colonies horizontal transmission also occurs and that infected flies secrete the virus during membrane feeding,
ii- utilized PCR-based detection tools and showed that tsetse colonies with low prevalence of SGH symptoms (approx. 5%) harbour high levels (80-100%) of asymptomatic infections, iii- determined (by qPCR) that asymptomatic flies (i.e., infected flies that do not show SGH symptoms) contain variable levels of GpSGHV,
iv- discovered that in colonies, membrane feeding facilitates horizontal virus transmission resulting in infected F1 progeny.
c. SGH symptom free colonies maintained:
partially achieved,
i- discovered that the tsetse fly virus exists in both an asymptomatic and symptomatic state whereas the house fly virus expresses only symptomatic infections,
ii- associated symptomatic GpSGHV infection with reduced fertility of both sexes,
iii- surveyed field populations throughout Africa to determine the prevalence of both symptomatic (by dissection) and asymptomatic (by PCR) infections in flies; prevalence determined by PCR varied widely (0-90%) among and within different Glossina spp,
iv- designed and tested different strategies to manage virus levels in tsetse colonies: clean feeding (i.e., fresh blood membranes are used for each feeding), RNAi, polyclonal antibodies, oligopeptides, and antiviral drugs; each of these strategies reduced virus loads to varying degrees,
v- found that integrating several strategies (such as clean feeding and antiviral drugs) eliminated symptomatic infections and significantly reduced the levels of asymptomatic infections in tsetse colonies.
5-Develop parasite refractory lines:
partially achieved because of the inability to efficiently transmit Sodalis between generations, nevertheless, we have:
i- identified tsetse endosymbiont transmission routes, and
ii- development of symbiont-based expression system.
6-Identify trypanosome inhibitory products:
produced anti-trypanosome nanobodies.
7-Incorporate parasite resistance traits into SIT lines:
could not be achieved in the time frame of this CRP (see point 5, because 7 depends on the achievement of 5).
8-Cytoplasmic incompatibility-mediated gene drive system:
i- discovered the presence of chromosomal insertions of Wolbachia symbionts in many tsetse species,
ii- discovered low titer Wolbachia infections in natural populations and colonies,
iii- determined tsetse Wolbachia genome sequences,
iv- discovered polyandry in natural tsetse populations.
9-Harness cytoplasmic incompatibility for SIT application:
i. discovered the functional role of Wolbachia in inducing high CI,
ii- A mathematical model was developed to use CI for paratransgenic application to derive desirable phenotypes.
10-Disseminate discoveries to endemic countries and interested parties and relevant databases:
i- we have built capacity in Tsetse & Trypanosome Research in participating DECs in Africa. This includes:
- Training of 6 PhD students and 8 research fellows from DECs in collaborating laboratories,
- Training of DEC researchers in collaborating laboratories through short-term visits,
- Presentations of research findings by DEC scientists in international meetings,
- Ability to recruit independent research funds to DEC scientists in collaboration with participating scientists and laboratories,
- Promote development of genomics knowledge, including genome sequencing and functional studies in multiple tsetse species through participating in International Glossina Genome Initiative.
11-Publish results in scientific journals:
See research publication list.
Relevance
The results of the CRP are very relevant to ongoing technology transfer activities in support of technical cooperation projects in Sub-Saharan Africa. The technical information generated by this CRP will contribute to improving SIT technology through a better understanding of the role that microbes play in the laboratory and field biology of tsetse. The goal is to improve the quality of decision making related to field implementation of SIT projects. The emphasis on the field component of the CRP will ensure effective transfer of technology and effective capacity building.
CRP Publications
Journal Articles under review (for the special issue of the Journal of Invertebrate Pathology) A. Research articles: 1. Balmand, S., Lohs, C., Aksoy, S., Heddi, A., Tissue distribution and transmission routes for the Tsetse fly endosymbionts. Journal of Invertebrate Pathology . 2012. 2. Boucias, D.G., Deng, F., Hu, Z., Garcia-Maruniak, A., Lietze, V.U., Immunological analysis of structural proteins from the Musca domestica salivary gland hypertrophy virus. Journal of Invertebrate Pathology . 2012. 3. Guerra, L., Stoffolano, J.G., Jr., Gambellini, G., Masci, V.L., Belardinelli, M.C., Fausto, A.M., Ultrastructure of the salivary glands of non-infected and infected glands in Glossina pallidipes by the salivary gland hypertrophy virus (SGHV). Journal of Invertebrate Pathology . 2012. 4. Kariithi, H.M., Ahmadi, M., Parker, A.G., Franz, G., Ros, V.I.D., Haq, I., Elashry, A.M., Vlak, J.M., Bergoin, M., Vreysen, M.J.B., Abd-Alla, A.M.M., Prevalence and genetic variation of salivary gland hypertrophy virus in wild populations of the tsetse fly Glossina pallidipes from southern and eastern Africa. Journal of Invertebrate Pathology . 2012. 5. Schneider, D.I., Garschall, K.I., Parker, A.G., Abd-Alla, A.M.M., Miller, W.J., Global Wolbachia prevalence, titer fluctuations and their potential of causing cytoplasmic incompatibilities in tsetse flies and hybrids of Glossina morsitans subgroup species. Journal of Invertebrate Pathology . 2012. 6. Tchouomene-Labou, J., Nana-Djeunga, H., Simo, G., Njitchouang, G.R., Cuny, G., Asonganyi, T., Njiokou, F., Transmission of sleeping sickness in the Bipindi focus of Cameroon: influence of seasonal and biotope-type variations on the entomological and parasitological parameters. Journal of Invertebrate Pathology . 2012. 7. Wang, J., Brelsfoard, C., Wu, Y., Aksoy, S., Intercommunity effects on microbiome and GpSGHV density regulation in tsetse flies. Journal of Invertebrate Pathology . 2012. B. Mini Reviews: 8. Abd-Alla, A., Bergoin, M., Parker, A., Maniania, N.K., Vlak, J.M., Bourtzis, K., Aksoy, S., Improving sterile insect technique (SIT) for tsetse flies through research on their symbionts and pathogens. Journal of Invertebrate Pathology . 2012. 9. Arif, B., Pavlik, L., Insect cell culture: Virus replication and applications in Biotechnology. Journal of Invertebrate Pathology . 2012. 10. Burand, J.P., Hunter, W.B., RNAi future in insect management. Journal of Invertebrate Pathology . 2012. 11. Caljon, G., De Vooght, L., Van Den Abbeele, J., Options for the delivery of anti-pathogen molecules in arthropod vectors. Journal of Invertebrate Pathology . 2012. 12. Doudoumis, V., Alatalo, R., Aksoy, E., Abd-Alla, A., Tsiamis, G., Brelsfoard, C., Aksoy, S., Bourtzis, K., Tsetse-Wolbachia Symbiosis: comes of ageand has great potential for pest and disease control. Journal of Invertebrate Pathology . 2012. 13. Holmes, P., Tsetse-transmitted trypanosomes-their biology, disease impact and control. Journal of Invertebrate Pathology . 2012. 14. Jehle, J.A., Abd-Alla, A.M.M., Wang, Y., Phylogeny and evolution of Hytrosaviridae. Journal of Invertebrate Pathology . 2012. 15. Kariithi, H.M., Van lent, J., van Oers, M.M., Abd-Alla, A.M.M., Vlak, J.M., Proteomic footprints of a Glossinavirus (Hytrosaviridae): An expeditious approach to virus control strategies in tsetse factories. Journal of Invertebrate Pathology . 2012. 16. Lietze, V.-U., Keesling, J.E., Lee, J.A., Vallejo, C.R., Geden, C., Boucias, D.G., Muscavirus disease dynamics in house fly populations – How is this virus transmitted and has it potential as a biological control agent? Journal of Invertebrate Pathology . 2012. 17. Malele, I., Mananqwa, O., Nyingilili, H.H., Kiwika, W.A., Lyaruu, E.A., Msangi, A.R., Ouma, J.O., Nkwengulila, G., Abd-Alla, A.M.M., Prevalence of SGHV among tsetse species of economic importance in Tanzania and their implication for SIT application. Journal of Invertebrate Pathology . 2012. 18. Maniania, N.K., Ekesi, S., The use of entomopathogenic fungi in the control of tsetse flies. Journal of Invertebrate Pathology . 2012. 19. Van Den Abbeele, J., Bourtzis, K., Weiss, B., Cordon-Rosales, C., Miller, W., Abd-Alla, A., Parker, A.G., Enhancing Tsetse fly refractoriness to Trypanosome infection - A new IAEA Coordinated Research Project. Journal of Invertebrate Pathology . 2012. 20. Vreysen, M.J.B., Seck, M.T., Sall, B., Bouyer, J., Tsetse flies: their biology and control using area-wide integrated pest management approaches. Journal of Invertebrate Pathology . 2012. Articles published by the CRP participant during the CRP period (2007-2012) Book Chapters:Abd-Alla, A.M.M., Boucias, D.G., Bergoin, M., 2010. Hytrosaviruses: Structure and genomic properties, in: Asgari, S., Johnson, K.N. (Eds.), Insect Virology. Caister Academic Press, Norfolk, pp. 103-121. Reviews: Gross, R., Vavre, F., Heddi, A., Hurst, G.D., Zchori-Fein, E., Bourtzis, K., 2009. Immunity and symbiosis. Mol Microbiol 73, 751-759. Heddi, A., 2009. Immunity says "yes" to symbiotic bacteria but keeps them under control! Biofutur 28, 36-39. Lietze, V.U., Abd-Alla, A.M.M., Vreysen, M.J.B., Geden, C.J., Boucias, D.G., 2010. Salivary gland hypertrophy viruses: a novel group of insect pathogenic viruses. Annu. Rev. Entomol. 56, 63-80.Scolari, F., Siciliano, P., Gabrieli, P., Gomulski, L.M., Bonomi, A., Gasperi, G., Malacrida, A.R., 2011. Safe and fit genetically modified insects for pest control: from lab to field applications. Genetica 139, 41-52. Weiss, B., Aksoy, S., 2011. Microbiome influences on insect host vector competence. Trends Parasitol. 27, 514-522. Research Articles: 7. Abd-Alla, A.M.M., Cousserans, F., Parker, A.G., Jehle, J.A., Parker, N.J., Vlak, J.M., Robinson, A.S., Bergoin, M., 2008. Genome analysis of a Glossina pallidipes salivary gland hypertrophy virus (GpSGHV) reveals a novel large double-stranded circular DNA virus. J. Virol. 82, 4595-4611. 8. Abd-Alla, A.M.M., Salem, T.Z., Parker, A.G., Wang, Y., Jehle, J.A., Vreysen, M.J.B., Boucias, D., 2011. Universal primers for rapid detection of Hytrosaviruses. J. Virol. Methods 171, 280-283. 9. Abd-Alla, A.M.M., Vlak, J.M., Bergoin, M., Maruniak, J.E., Parker, A.G., Burand, J.P., Jehle, J.A., Boucias, D.G., 2009. Hytrosaviridae: a proposal for classification and nomenclature of a new insect virus family. Arch. Virol. 154, 909-918. 10. Alam, U., Medlok, J., Brelsfoard, C., Pais, R., Lohs, C., Balmand, S., Carnogursky, J., Heddi, A., Takac, P., Galvani, A., Aksoy, S., 2011. Wolbachia symbiont infections induce strong Cytoplasmic icompatibility in the tsetse fly Glossina morsitans. PLoS Pathog. 7, e1002415. 11. Anselme, C., Perez-Brocal, V., Vallier, A., Vincent-Monegat, C., Charif, D., Latorre, A., Moya, A., Heddi, A., 2008. Identification of the weevil immune genes and their expression in the bacteriome tissue. BMC Biol 6, 43. 12. Apostolaki, A., Livadaras, I., Saridaki, A., Chrysargyris, A., Savakis, C., Bourtzis, K., 2011. Transinfection of the olive fruit fly Bactrocera oleae with Wolbachia: towards a symbiont-based population control strategy. J. Appl. Entomol. 135, 1-8. 13. Attardo, G.M., Strickler-Dinglasan, P., Perkin, S.A.H., Caler, E., Bonaldo, M.F., Soares, M.B., El Sayeed, N., Aksoy, S., 2006. Analysis of fat body transcriptome from the adult tsetse fly, Glossina morsitans morsitans. Insect Mol. Biol. 15, 411-424. 14. Bonomi, A., Bassetti, F., Gabrieli, P., Beadell, J., Falchetto, M., Scolari, F., Gomulski, L.M., Regazzini, E., Ouma, J.O., Caccone, A., Okedi, L.M., Attardo, G.M., Guglielmino, C.R., Aksoy, S., Malacrida, A.R., 2011. Polyandry is a common event in wild populations of the tsetse fly Glossina fuscipes fuscipes and may impact population reduction measures. PLoS Negl. Trop Dis 5, e1190. 15. Bordenstein, S.R., Paraskevopoulos, C., Dunning Hotopp, J.C., Sapountzis, P., Lo, N., Bandi, C., Tettelin, H., Werren, J.H., Bourtzis, K., 2009. Parasitism and mutualism in Wolbachia: what the phylogenomic trees can and cannot say. Mol Biol Evol 26, 231-241. 16. Bourtzis, K., 2008. Wolbachia-based technologies for insect pest population control, in: Aksoy, S. (Ed.), Transgenesis and the Management of Vector-Borne Disease ( Advances in Experimental Medicine and Biology ). Springer Science+Business Media, LLC 233 Springer Street, New York, New York 10013, USA ( www.springer.com ), New York, pp. 104-113. 17. De Vooght, L., Caljon, G., Stijlemans, B., De Baetselier, P., Coosemans, M., Van Den, A.J., 2012. Expression and extracellular release of a functional anti-trypanosome Nanobody(R) in Sodalis glossinidius, a bacterial symbiont of the tsetse fly. Microb Cell Fact 11, 23. 18. De Vooght, L., Caljon.G., Coosemans, M., Abbeele, J.v.d., 2011. Functional analysis of the twin-arginine translocation pathway in Sodalis glossinidius, a bacterial symbiont of the tsetse fly. Appl. Env. Microbiol. 77, 1132-1134. 19. Doudoumis, V., Tsiamis, G., Wamwiri, F., Brelsfoard, C., Alam, U., Aksoy, E., Dalaperas, S., Abd-Alla, A., Ouma, J., Takac, P., Aksoy, S., Bourtzis, K., 2012. Detection and characterization of Wolbachia infections in laboratory and natural populations of different species of tsetse flies (genus Glossina). 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First isolation of Enterobacter, Enterococcus, and Acinetobacter spp. as inhabitants of the tsetse fly (Glossina palpalis papalis) midgut. Infection, Genetics and Evolution 9, 1364-1370. 31. Geiger, A., Fardeau, M.L., Njiokou, F., Joseph, M., Asonganyi, T., Ollivier, B., Cuny, G., 2011. Bacterial diversity associated with populations of Glossina spp. from Cameroon and distribution within the Campo sleeping sickness focus. Microbial Ecology 62, 632-643. 32. Gerardo, N.M., Altincicek, B., Anselme, C., Atamian, H., Barribeau, S.M., de Vos, M., Duncan, E.J., Evans, J.D., Gabaldon, T., Ghanim, M., Heddi, A., Kaloshian, I., Latorre, A., Moya, A., Nakabachi, A., Parker, B.J., Perez-Brocal, V., Pignatelli, M., Rahbe, Y., Ramsey, J.S., Spragg, C.J., Tamames, J., Tamarit, D., Tamborindeguy, C., Vincent-Monegat, C., Vilcinskas, A., 2010. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 11, R21. 33. 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Klasson, L., Westberg, J., Sapountzis, P., Naslund, K., Lutnaes, Y., Darby, A.C., Veneti, Z., Chen, L., Braig, H.R., Garrett, R., Bourtzis, K., Andersson, S.G., 2009. The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci U S A 106, 5725-5730. 42. Lietze, V.U., Abd-Alla, A.M., Boucias, D.G., 2011a. Two hytrosaviruses, MdSGHV and GpSGHV, induce distinct cytopathologies in their respective host insects. J. Invertebr. Pathol. 107, 161-163. 43. Lietze, V.U., Geden, C.J., Blackburn, P., Boucias, D.G., 2007. Effects of salivary gland hypertrophy virus on the reproductive behavior of the housefly, Musca domestica. Appl. Environ. Microbiol. 73, 6811-6818. 44. Lietze, V.U., Geden, C.J., Doyle, M.A., Boucias, D.G., 2011b. Disease dynamics and persistence of MdSGHV-infections in laboratory house fly (Musca domestica) populations. Appl. Environ. Microbiol. 78, 311-317. 45. Lietze, V.U., Salem, T.Z., Prompiboon, P., Boucias, D.G., 2011c. 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Special Issue
2012
Improving SIT for Tsetse Flies through Research on their Symbionts and Pathogens