Wolbachia, Sodalis and trypanosome co-infections in natural populations of Glossina austeni and Glossina pallidipes

Parasites and Vectors

Volumn 6, Issue 1, 2013, Pages

  Wamwiri, Florence N ^a   Alam, Uzma ^b   Thande, Paul C ^a   Aksoy, Emre ^b   Ngure, Raphael M ^c   Aksoy, Serap ^b   Ouma, Johnson O ^a   Murilla, Grace A ^a  

^a KENYA AGRICULTURAL RESEARCH INSTITUTE   (Kenya)

^b YALE UNIVERSITY   (United States)

^c EGERTON UNIVERSITY   (Kenya)

Author keywords

Co infection; Glossina; Kenya; Shimba Hills; Sodalis; Trypanosomes; Wolbachia

Indexed keywords

AGE DISTRIBUTION; ARTICLE; CONTROLLED STUDY; DENSITY; ENDOSYMBIONT; ENVIRONMENTAL FACTOR; FEMALE; FOREST; GENE AMPLIFICATION; GLOSSINA; GLOSSINA AUSTENI; GLOSSINA PALLIDIPES; GRAM NEGATIVE BACTERIUM; LIFESPAN; MALE; MICROSCOPY; MIDGUT; MIXED INFECTION; NATURAL POPULATION; NONHUMAN; PARASITOSIS; POLYMERASE CHAIN REACTION; SODALIS; TRYPANOSOMATID INFECTION; TRYPANOSOMIASIS; WOLBACHIA;

BACTERIA (MICROORGANISMS); GLOSSINA (GENUS); GLOSSINA AUSTENI; GLOSSINA PALLIDIPES; SODALIS; SODALIS GLOSSINIDIUS; WIGGLESWORTHIA; WIGGLESWORTHIA GLOSSINIDIA; WOLBACHIA; WOLBACHIA PIPIENTIS;

EID: 84881176632     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-6-232     Document Type: Article

References (69)

1. Partnerships for tsetse control: community participation and other options. Barrett K, Okali C, World Anim Rev 1998 90 39 46
2. Tsetse-typanosome interactions: rites of passage. Welburn SC, Maudlin I, Parasitol Today 1999 15 399 403 10.1016/S0169-4758(99)01512-4 10481151
3. Interactions between tsetse and trypanosomes with implications for the control of trypanosomiasis. Aksoy S, Gibson WC, Lehane MJ, Adv Parasitol 2003 53 1 83 14587696
4. Tsetse immune responses and trypanosome transmission: implications for the development of tsetse-based strategies to reduce trypanosomiasis. Hao Z, Kasumba I, Lehane MJ, Gibson WC, Kwon J, Aksoy S, Proc Natl Acad Sci U S A 2001 98 22 12648 12653 10.1073/pnas.221363798 11592981
5. Sterility in tsetse flies Glossina morsitans Westwood caused by loss of symbionts. Nogge G, Experientia 1976 32 995 996 10.1007/BF01933932 986317
6. Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Wang J, Wu Y, Yang G, Aksoy S, Proc Natl Acad Sci USA 2009 106 29 12133 12138 10.1073/pnas.0901226106 19587241
7. The Obligate Mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Pais R, Lohs C, Wu Y, Wang J, Aksoy S, Appl Environ Microbiol 2008 74 5965 5974 10.1128/AEM.00741-08 18689507
8. The tsetse fly Glossina fuscipes fuscipes (Diptera: Glossina) harbours a surprising diversity of bacteria other than symbionts. Lindh JM, Lehane MJ, Antonie Leeuwenhoek 2011 99 711 720 10.1007/s10482-010-9546-x 21203841
9. Microfauna-host interactions: implications for trypanosome transmission dynamics in Glossina fuscipes fuscipes in Uganda. Alam U, Hyseni C, Symula RE, Brelsfoard C, Wu Y, Kruglov O, Wang J, Echodu R, Alioni V, Okedi LM, Caccone A, Aksoy S, Appli Environ Microbiol 2012 78 13 4627 4637 10.1128/AEM.00806-12
10. Tripartite interactions between tsetse flies, Sodalis glossinidius and trypanosomes-An epidemiological approach in two historical human African trypanosomiasis foci in Cameroon. Farikou O, Njiokou F, Mbida JAM, Njitchouang GR, Djeunga HN, Asonganyi T, Simarro PP, Cuny G, Geiger A, Infect Genet Evol 2010 10 115 121 10.1016/j.meegid.2009.10.008 19879380
11. Vector competence of Glossina palpalis gambiensis for Trypanosoma brucei s.l. and genetic diversity of the symbiont Sodalis glossinidius. Geiger A, Ravel S, Mateille T, Janelle J, Patrel D, Cuny G, Frutos R, Mol Biol Evol 2007 24 102 109 17012373
12. Microbiome influences on insect host vector competence. Weiss B, Aksoy S, Trends Parasitol 2011 27 11 514 522 10.1016/j.pt.2011.05.001 21697014
13. Obligate symbionts activate immune system development in the tsetse fly. Weiss BL, Maltz M, Aksoy S, J Immunol 2012 188 7 3395 3403 10.4049/jimmunol. 1103691 22368278
14. Bacterial symbionts of the Triatomine and their potential use in control of Chagas disese transmission. Beard CB, Cordon-Rosales C, Durvasula RV, Annu Rev Entomol 2002 47 123 141 10.1146/annurev.ento.47.091201.145144 11729071
15. The paratransgenic sand fly: a platform for control of Leishmania transmission. Hurwitz I, Hillesland H, Fieck A, Das P, Durvasula R, Parasit Vectors 2011 19 4 82
16. Using bacteria to express and display anti-Plasmodium molecules in the mosquito midgut. Riehle MA, Moreira CK, Lampe D, Lauzon C, Jacobs-Lorena M, Int J Parasitol 2007 37 595 603 10.1016/j.ijpara.2006.12.002 17224154
17. Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: a step toward finding suitable paratransgenesis candidates. Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA, Mardani N, Ghoorchian S, Acta Trop 2012 121 129 134 10.1016/j.actatropica.2011.10.015 22074685
18. Using infections to fight infections: paratransgenic fungi can block malaria transmission in mosquitoes. Rasgon JL, Future Microbiol 2011 6 851 853 10.2217/fmb.11.71 21861618
19. Eradication of Culex pipiens fatigans through Cytoplasmic Incompatibility. Laven H, Nature 1967 216 383 384 10.1038/216383a0 4228275
20. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Zabalou S, Riegler M, Theodorakopoulou M, Savakis C, Bourtzis K, Proc Natl Acad Sci USA 2004 101 15042 15045 10.1073/pnas.0403853101 15469918
21. Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the tsetse fly Glossina morsitans. Alam U, Medlock J, Brelsfoard C, Pais R, Lohs C, Balmand S, Carnogursky J, Heddi A, Takac P, Galvani A, Aksoy S, PLoS Pathog 2011 7 12 1002415 10.1371/journal.ppat.1002415 22174680
22. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and death. Min KT, Benzer S, Proc Natl Acad Sci USA 1997 94 10792 10796 10.1073/pnas.94.20.10792 9380712
23. Modifying insect population age structure to control vector-borne disease. Cook PE, McMeniman CJ, O'Neill SL, Adv Exp Med Biol 2008 627 126 140 10.1007/978-0-387-78225-6-11 18510020
24. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya and Plasmodium. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Bruno R, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, van de Hurk AF, Ryan P, O'Neill SL, Cell 2009 139 7 1268 1278 10.1016/j.cell.2009.11.042 20064373
25. Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. van den Hurk AF, Hall-Mendelin S, Pyke AT, Frentiu FD, McElroy K, Day A, Higgs S, O'Neill SL, PLoS Negl Trop Dis 2012 6 1892 10.1371/journal.pntd.0001892 23133693
26. Wolbachia and the biological control of mosquito-borne disease. Iturbe-Ormaetxe I, Walker T, Neill SLO, EMBO Rep 2011 12 6 508 518 10.1038/embor.2011.84 21546911
27. Microbe-induced cytoplasmic incompatibility as a mechanism for introducing transgenes into arthropods populations. Turelli M, Hoffmann AA, Insect Biochem Mol Biol 1999 8 243 255 10.1046/j.1365-2583.1999.820243.x
28. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Cheng Q, Ruel TD, Zhou W, Moloo SK, Majiwa P, O'Neill SL, Aksoy S, Med Vet Entomol 2000 14 44 50 10.1046/j.1365-2915.2000.00202.x 10759311
29. Un nouveau piege pour la capture des glossines (Glossina: Diptera, Muscidae): description et essays sur le terrain. Challier A, Laveissiere C, Cahiers ORSTOM, series Entomologie Medical Parasitologie 1973 11 251 262
30. A new trap for Glossina pallidipes. Brightwell R, Dransfield RD, Kyorku C, Golder TK, Tarimo SA, Mungai D, Trop Pest Manag 1987 33 151 189 10.1080/09670878709371136
31. Responses of Glossina austeni to sticky panels and odours. Vreysen MJB, Saleh KM, Zhu Z-R, Suleiman FW, Med Vet Entomol 2000 14 283 289 10.1046/j.1365-2915.2000.00241.x 11016436
32. Improved persistence of insecticide deposits on targets for controlling Glossina pallidipes (Diptera: Glossinidae). Torr SJ, Holloway MTP, Vale GA, Bull Entomol Res 1992 82 525 533 10.1017/S0007485300042620
33. Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Sunnucks P, Hales DF, Mol Biol Evol 1996 13 510 524 10.1093/oxfordjournals.molbev.a025612 8742640
34. Cloning and characterisation of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. Braig HR, Zhou W, Dobson S, O'Neill S, J Bacteriol 1998 180 2373 2378 9573188
35. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Zhou WG, Rousset F, O'Neill S, Proc R Soc Lond B Biol Sci 1998 265 509 515 10.1098/rspb.1998.0324
36. Detection and characterization of Wolbachia infections in laboratory and natural populations of different species of tsetse flies (genus Glossina). Doudoumis V, Tsiamis G, Wamwiri F, Brelsfoard C, Alam U, Aksoy E, Dalaperas S, Abd-Alla AMM, Ouma J, Takac P, Aksoy S, Bourtzis K, BMC Microbiol 2012 12 3 10.1186/1471-2180-12-S1-S3 22376025
37. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Dale C, Maudlin I, Int J Syst Bacteriol 1999 49 267 275 10.1099/00207713-49-1-267 10028272
38. Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P, Ann Entomol Soc Am 1994 87 651 704
39. The trypanosome infections of tsetse flies in Northern Nigeria and a new method of estimation. Lloyd L, Johnson WB, Bull Entomol Res 1924 14 265 288
40. The use of ITS1 rDNA PCR in detecting pathogenic African trypanosomes. Njiru ZK, Constantine CC, Guya S, Crowther J, Kiragu JM, Thompson RC, Dávila AM, Parasitol Res 2005 95 3 186 192 10.1007/s00436-004-1267-5 15619129
41. An artificially isolated generation of tsetse flies (Diptera). Jackson CHN, Bull Entomol Res 1946 37 291 299 10.1017/S0007485300022203 21000966
42. Age determination for female tsetse flies and the age compositions of samples of Glossina pallidipes Austen, G. palpalis fuscipes Newst. and G.brevipalpis Newst. Saunders DS, Bull Entomol Res 1962 53 579 595 10.1017/S0007485300048331
43. Studies on the biconical trap as a sampling device for tsetse (Diptera: Glossinidae) in Mozambique. Takken W, Int J Trop Insect Sci 1984 5 357 361 10.1017/S1742758400008663
44. An update on the utility of Wolbachia for controlling insect vectors and disease transmission. Brelsfoard CL, Dobson SL, AsPac J Mol Biol Biotechnol 2011 19 3 85 92
45. Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Clancy DJ, Hoffmann AA, Entomol Exp Appl 1998 86 13 24 10.1046/j.1570-7458.1998.00261.x
46. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Mouton L, Henri H, Charif D, Boulétreau M, Vavre F, Biol Lett 2007 3 2 210 213 10.1098/rsbl.2006.0590 17251124
47. Hiden Wolbachia diversity in field populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae). Arthofer W, Riegler M, Schneider D, Krammer M, Miller WJ, Mol Ecol 2009 18 3816 3830 10.1111/j.1365-294X.2009.04321.x 19732336
48. Deciphering Wolbachia diversity in Glossina spp. Miller WJ, Schneider D, Improving SIT for tsetse flies through research on their symbionts and pathogens: 2010 Nairobi, Kenya: IAEA 2010
49. Infection density of Wolbachia and level of cytoplasmic incompatibility in the Mediterranean flour moth, Ephestia kuehniella. Ikeda T, Ishikawa H, Sasaki T, J Invertebr Pathol 2003 84 1 5 10.1016/S0022-2011(03)00106-X 13678706
50. In vitro cultivation of Wolbacha pipientis in an Aedes albopictus cell line. O'Neill S, Pettigrew M, Sinkins S, Braig HR, Andreadis T, Tesh R, Insect Mol Biol 1997 6 33 39 10.1046/j.1365-2583.1997.00157.x 9013253
51. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. McMeniman CJ, Lane RV, Cass BN, Fong AW, Sidhu M, Wang YF, O'Neill SL, Science 2009 323 141 144 10.1126/science.1165326 19119237
52. Tsetse salivary gland hypertrophy virus: hope or hindrance for tsetse control? Abd-Alla AMM, Parker AG, Vreysen MJB, Bergoin M, PLoS Negl Trop Dis 2011 5 8 1220 10.1371/journal.pntd.0001220 21912708
53. Costs and Benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Russel JA, Moran NA, Proc R Soc Lond 2006 273 603 610 10.1098/rspb.2005.3348
54. Dynamics of multiple symbiont density regulation during host development: tsetse fly and its microbial flora. Rio RV, Wu YN, Filardo G, Aksoy S, Proc R Soc Lond B Biol Sci 2006 273 805 814 10.1098/rspb.2005.3399
55. The relationship between rickettsia-like organisms and trypanosome infections in natural populations of tsetse in Liberia. Maudlin I, Welburn SC, Mehlitz D, Trop Med Parasitol 1990 41 265 267 2255842
56. Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Toju H, Fukatsu T, Mol Ecol 2011 20 4 853 868 10.1111/j.1365-294X.2010.04980.x 21199036
57. GoK, The 2010 Short Rains Season Assessment Report Nairobi: Government of Kenya 2011 40
58. Tsetse: a haven for microorganisms. Aksoy S, Parasitol Today 2000 16 114 118 10.1016/S0169-4758(99)01606-3 10689331
59. Trypanosome infections in wild tsetse, Glossina pallidipes Austen on the Kenya coast. Tarimo SA, Snow WF, Butler L, Int J Trop Insect Sci 1984 5 05 415 418 10.1017/S1742758400008754
60. Livestock farmers' perception and epidemiology of bovine trypanosomiasis in Kwale District, Kenya. Ohaga SO, Kokwaro ED, Ndiege IO, Hassanali A, Saini RK, Prev Vet Med 2007 80 24 33 10.1016/j.prevetmed.2007.01.007 17324481
61. Vector competence of Glossina austeni and Glossina brevipalpis for Trypanosoma congolense in KwaZulu-Natal, South Africa. Motloang M, Masumu J, Mans B, Van den Bossche P, Latif A, Onderstepoort J Vet Res 2012 79 1 1 e6 23327410
62. Multiple Trypanosoma infections are common amongst Glossina species in the new farming areas of Rufiji district, Tanzania. Malele II, Magwisha HB, Nyingilili HS, Mamiro KA, Rukambile EJ, Parasit Vectors 2011 4 217 10.1186/1756-3305-4-217 22093363
63. Identification of different trypanosome species in the mid-guts of tsetse flies of the Malanga (Kimpese) sleeping sickness focus of the Democratic Republic of Congo. Simo G, Silatsa B, Njiokou F, Lutumba P, Mansinsa P, Madinga J, Manzambi E, De Deken R, Asonganyi T, Parasit Vectors 2012 5 201 10.1186/1756-3305-5-201 22992486
64. Identification of trypanosomes in Glossina pallidipes and G. longipennis in Kenya. Njiru ZK, Makumi JN, Okoth S, Ndungu JM, Gibson WC, Infect Genet Evol 2003 4 29 35
65. Tissue tropism, transmission and expression of foreign genes in vivo in midgut symbionts of tsetse flies. Cheng Q, Aksoy S, Insect Mol Biol 1999 8 125 132 10.1046/j.1365-2583.1999.810125.x 9927181
66. Haemagglutinins and parasite agglutinins in heamolymph and gut of Glossina. Ibrahim EAR, Ingram GA, Molyneux DH, Trop Med Parasitol 1984 35 151 156
67. Sodalis glossinidius (Enterobacteriaceae) and vectorial competence of Glossina palpalis gambiense and Glossina morsitans morsitans for Trypanosoma congolense savannah type. Geiger A, Ravel S, Frutos R, Cuny G, Curr Microbiol 2005 51 1 35 40 10.1007/s00284-005-4525-6 15942697
68. Interspecific transfer of bacterial endosymbionts between tsetse fly species: infection establishment and effect on host fitness. Weiss BL, Mouchotte R, Rio RV, Wu YN, Wu Z, Heddi A, Aksoy S, Appl Environ Microbiol 2006 72 7013 7021 10.1128/AEM.01507-06 16950907
69. Rickettsia-like organisms and chitinase production in relation to transmission of trypanosomes by tsetse flies. Welburn SC, Arnold K, Maudlin I, Gooday GW, Parasitol 1993 107 141 145 10.1017/S003118200006724X