The bacterial flora of tsetse fly midgut and its effect on trypanosome transmission

Journal of Invertebrate Pathology

Volumn 112, Issue SUPPL.1, 2013, Pages

  Hamidou Soumana, Illiassou ^a   Simo, Gustave ^b   Njiokou, Flobert ^c   Tchicaya, Bernadette ^a   Abd Alla, Adly M M ^d   Cuny, Gérard ^a   Geiger, Anne ^a  

^a CIRAD   (France)

^b UNIVERSITY OF DSCHANG   (Cameroon)

^c UNIVERSITY OF YAOUNDÉ I   (Cameroon)

^d INTERNATIONAL ATOMIC ENERGY AGENCY   (Austria)

Author keywords

Diversity; Fitness; Microbiota; Sleeping sickness; Tsetse fly; Vector competence

Indexed keywords

AFRICAN TRYPANOSOMIASIS; ANIMAL; CATTLE; DISEASE CARRIER; DISEASE TRANSMISSION; GLOSSINIDAE; HUMAN; INTESTINE; MICROBIOLOGY; PARASITOLOGY; REVIEW; SYMBIOSIS; TRYPANOSOMA;

ANIMALS; CATTLE; HUMANS; INSECT VECTORS; INTESTINES; SYMBIOSIS; TRYPANOSOMA; TRYPANOSOMIASIS, AFRICAN; TSETSE FLIES;

ACINETOBACTER; BACTERIA (MICROORGANISMS); BOS; ENTEROCOCCUS; GLOSSINA (GENUS); GLOSSINA PALPALIS; GLOSSINIDAE; HEXAPODA; SODALIS; SODALIS GLOSSINIDIUS; TRYPANOSOMA; VERTEBRATA; WIGGLESWORTHIA; WOLBACHIA;

EID: 84875808479     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2012.03.029     Document Type: Review

References (59)

1. Abd-Alla A.M., Parker A.G., Vreysen M.J., Bergoin M. Tsetse salivary gland hypertrophy virus: hope or hindrance for tsetse control? PLoS Negl. Trop. Dis. 2011, 5:e1220.
2. Akman L., Yamashita A., Watanabe H., Oshima K., Shiba T., Hattori M., Aksoy S. Genome sequence of the endocellular obligate symbiont of tsetse, Wigglesworthia glossinidia. Nat. Genet. 2002, 32:402-407.
3. Aksoy S. Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int. J. Syst. Bacteriol. 1995, 45:848-851.
4. 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.
5. Azambuja P., Feder D., Garcia E.S. Isolation of Serratia marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Exp. Parasitol. 2004, 107:89-96.
6. Beier M.S., Pumpuni C.B., Bizio J.C., Davis J.R. Effect of paraaminobenzenoic acid, insulin, and gentamicin on Plasmodium falciparum development in Anopheline mosquitoes (Diptera: Culicidae). J. Med. Entomol. 1994, 31:561-565.
7. Brummel T., Ching A., Seroude L., Simon A.F., Benzer S. Drosophila lifespan enhancement by exogenous bacteria. Proc. Natl. Acad. Sci. USA 2004, 101:12974-12979.
8. Cheng Q., Aksoy A. Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Insect Mol. Biol. 1999, 8:125-132.
9. Chen X., Song L., Aksoy A. 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.
10. 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.
11. Dale C., Welburn S.C. The endosymbionts of tsetse flies: manipulating host-parasite interactions. Int. J. Parasitol. 2001, 31:628-631.
12. Farikou O., Njiokou F., Mbida Mbida J.A., Njitchouang G.R., Nana Djeunga H., Asonganyi T., Simarro P.P., 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.
13. Farikou O., Njiokou F., Simo G., Asonganyi T., Cuny G., Geiger A. Tsetse fly blood meal modification and trypanosome identification in two sleeping sickness foci in the forest of southern Cameroon. Acta Trop. 2010, 116:81-88.
14. Farikou O., Thevenon S., Njiokou F., Allal F., Cuny G., Geiger A. Genetic diversity and population structure of the secondary symbiont of tsetse flies, Sodalis glossinidius, in sleeping sickness foci in Cameroon. PLoS Negl. Trop. Dis. 2011, 5:e1281.
15. Fèvre E.M., Wissmann B.V., Welburn S.C., Lutumba P. The burden of human African trypanosomiasis. PLoS Negl. Trop. Dis. 2008, 2:e333.
16. Fukatsu T., Koga R., Smith W.A., Tanaka K., Nikoh N., Sasaki-Fukatsu K., Yoshizawa K., Dale C., Clayton D.H. Bacterial endosymbiont of the slender pigeon louse, Columbicola columbae, allied to endosymbionts of grain weevils and tsetse flies. Appl. Environ. Microbiol. 2007, 73:6660-6668.
17. 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.
18. Geiger A., Ravel S., Mateille T., Janelle J., Patrel D., Cuny G., Frutos R. Vector competence of Glossina palpalis gambiensis for Trypanosoma brucei s.l. and genetic diversity of the symbiont Sodalis glossinidius. Mol. Biol. Evol. 2007, 24:102-109.
19. Geiger A., Fardeau M.L., Grebaut P., Vatunga G., Josénando T., Herder S., Cuny G., Truc P., Ollivier B. First isolation of Enterobacter, Enterococcus, and Acinetobacter spp. as inhabitants of the tsetse fly (Glossina palpalis palpalis) midgut. Infect. Genet. Evol. 2009, 9:1364-1370.
20. Geiger A., Fardeau M.L., Falsen E., Ollivier B., Cuny G. Serratia glossinae sp. nov., isolated from the midgut of the tsetse fly Glossina palpalis gambiensis. Int. J. Syst. Evol. Microbiol. 2010, 60:1261-1265.
21. Geiger A., Fardeau M.L., Njiokou F., Joseph M., Asonganyi T., Ollivier B., Cuny G. Bacterial diversity associated with populations of Glossina spp. from Cameroon and distribution within the campo sleeping sickness focus. Microb. Ecol. 2011, 62:632-643.
22. Glaser R.L., Meola M.A. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One 2010, 5:e11977.
23. Gonzalez-Ceron L., Santillan F., Rodriguez M.H., Mendez D., Hernandez-Avila J.E. Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J. Med. Entomol. 2003, 40:371-374.
24. Grünwald S., Pilhofer M., Höll W. Microbial associations in gut systems of wood- and bark-inhabiting longhorned beetles [Coleptera: Cerambycidae]. Syst. Appl. Microbiol. 2010, 33:25-34.
25. Hammes W., Hertel C. The genera Lactobacillus and Carnobacterium. The Prokaryotes 2006, 320-403. Springer, New York NY. M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, E. Stackebrandt (Eds.).
26. Heddi A., Nardon P. Sitophilus oryzae L.: a model for intracellular symbiosis in the Dryophthoridae weevils (Coleoptera). Symbiosis 2005, 39:1-11.
27. Hotez P.J., Fenwick A., Savioli L., Molyneux D.H. Rescuing the bottom billion through control of neglected tropical diseases. Lancet 2009, 373:1570-1575.
28. Jackson T.J., Wang H.Y., Nugent M.J., Griffin C.T., Burnell A.M., Dowds B.C.A. Isolation of insect pathogenic bacteria, Providencia rettgeri, from Heterorhabditis spp. J. Appl. Bacteriol. 1995, 78:237-244.
29. Kaaya G.P., Darji N. Mortality in adult tsetse, Glossina morsitans morsitans, caused by entomopathogenic bacteria. J. Invertebr. Pathol. 1989, 54:32-38.
30. Kaiwa N., Hosokawa T., Kikuchi Y., Nikoh N., Meng X.Y., Kimura N., Ito M., Fukatsu T. Primary gut symbiont and secondary, Sodalis-allied symbiont of the Scutellerid stinkbug Cantao ocellatus. Appl. Environ. Microbiol. 2010, 76:3486-3494.
31. Manual of Techniques in Insect Pathology 1997, Academic, San Diego, CA. L.A. Lacey (Ed.).
32. Lazaro J.E., Nitcheu J., Predicala R.Z., Mangalindan G.C., Nesslany F., Marzin D., Concepcion G.P., Diquet B. Heptyl prodigiosin, a bacterial metabolite is antimalarial in vivo and non-mutagenic in vitro. J. Nat. Toxins 2002, 11:367-377.
33. Lindh J.M., Lehane M.J. The tsetse fly Glossina fuscipes fuscipes (Diptera: Glossina) harbours a surprising diversity of bacteria other than symbionts. Antonie Van Leeuwenhoek. 2011, 99:711-720.
34. Lysyk T.J., Kalischuk-Tymensen L., Selinger L.B., Lancaster R.C., Wever L., Cheng K.J. Rearing stable fly larvae (Diptera: Muscidae) on an egg yolk medium. J. Med. Entomol. 1999, 36:382-388.
35. Mercado T.I., Colon-Whitt A. Lysis of Trypanosoma cruzi by Pseudomonas fluorescens. Antimicrob. Agents Ch. 1982, 22:1051-1057.
36. Moloo S.K. Mermithid parasite of Glossina brevipalpis Newstead. Ann. Trop. Med. Parasitol. 1972, 66:159.
37. Moreira L.A., Iturbe-Ormaetxe I., Jeffery J.A., Lu G., Pyke A.T., Hedges L.M., Rocha B.C., Hall-Mendelin S., Day A., Riegler M., Hugo L.E., Johnson K.N., Kay B.H., McGraw E.A., van Den Hurk A.F., Ryan P.A., O'Neill S.L. A Wolbachia symbiont in Aedes aegypti limits infection with Dengue, Chikungunya, and Plasmodium. Cell 2009, 139:1268-1278.
38. Moss M. Bacterial pigments. Microbiologist 2002, 3:10-12.
39. Novakova E., Hypsa V. A new Sodalis lineage from blood sucking fly Craterina melbae (Diptera, Hippoboscoidea) originated independently of tsetse flies symbiont Sodalis glossinidius. FEMS Microbiol. Lett. 2007, 269:131-135.
40. O'Neill S.L., Giordano R., Colbert A.M., Karr T.L., Robertson H.M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. 1992, 89:2699-2702.
41. O'Neill S.L., Gooding R.H., Aksoy S. Phylogenetically distant symbiotic microorganisms reside in Glossina midgut and ovary tissues. Med. Vet. Entomol. 1993, 7:377-383.
42. 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.
43. Pan X., Zhou G., Wu J., Bian G., Lu P., Raikhel A.S., Xi Z. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. 2012, 109:E23-E31.
44. Poinar G.O., Wassink H.J., Leegwater-van der Linden M.E., van der Geest L.P. Serratia marcescens as a pathogen of tsetse flies. Acta Trop. 1979, 36:223-227.
45. Pumpuni C.B., DeMaio J., Kent M., Davis J.R., Beier J.C. Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am. J. Trop. Med. Hyg. 1996, 54:214-218.
46. Reinhardt, E., 2002. Travailler ensemble: la mouche tsé-tsé et la pauvreté rurale. Chronique ONU; ONU Editor-September 02. Available from <>. http://www.un.org/french/pubs/chronique/2002/numero2/0202p17_la_mouche_tsetse.html.
47. Rio R.V., Hu Y., Aksoy S. Strategies of the home-team: symbioses exploited for vector-borne disease control. Trends Microbiol. 2004, 12:325-336.
48. Simarro P.P., Jannin J., Cattand P. Eliminating human African trypanosomiasis: where do we stand and what comes next?. PLoS Med. 2008, 5:e55.
49. Simo G., Njiokou F., Mbida Mbida J.A., Njitchouang G.R., Herder S., Asonganyi T., Cuny G. Tsetse fly host preference from sleeping sickness foci in Cameroon: epidemiological implications. Infect. Genet. Evol. 2008, 8:34-39.
50. Straif S.C., Mbogo C.N.M., Toure A.M., Walker E.D., Kaufman M., Toure Y.T., Beier J.C. Midgut bacteria in Anopheles gambiae and A. funestus (Diptera: Culicidae) from Kenya and Mali. J. Med. Entomol. 1998, 35:222-226.
51. Toju H., Hosokawa T., Koga R., Nikoh N., Meng X.Y., Kimura N., Fukatsu T. " Candidatus Curculioniphilus buchneri" , a novel clade of bacterial endocellular symbionts from weevils of the genus Curculio. Appl. Environ. Microbiol. 2010, 76:275-282.
52. Van Den Abbeele J., Claes Y., Bockstaele D., Ray D., Coosemans M. Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 1999, 118:469-478.
53. Vickerman K., Tetley L., Hendry A., Turner C.M. Biology of African trypanosomes in the tsetse fly. Biol. Cell 1988, 64:109-119.
54. Walker T., Johnson P.H., Moreira L.A., Iturbe-Ormaetxe I., Frentiu F.D., McMeniman C.J., Leong Y.S., Dong Y., Axford J., Kriesner P., Lloyd A.L., Ritchie S.A., O'Neill S.L., Hoffmann A.A. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 2011, 476:450-453.
55. Welburn S.C., Arnold K., Maudlin I., Gooday G.W. Rickettsia-like organisms and chitinase production in relation to transmission of trypanosomes by tsetse-flies. Parasitology 1993, 107:141-145.
56. Welburn S.C., Maudlin I. Tsetse-trypanosome interactions: rites of passage. Parasitol. Today 1999, 15:399-403.
57. Welburn S.C., Maudlin I., Simarro P.P. Controlling sleeping sickness - a review. Parasitology 2009, 136:1943-1949.
58. WHO, 2010. African Trypanosomiasis (Sleeping Sickness). Report of a WHO Expert Committee, 259. WHO Technical Report Series.
59. Zhou W., Rousset F., O'Neill S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. R. Soc. Lond. Ser. 1998, 265:509-515.