Glossina spp. Gut bacterial flora and their putative role in fly-hosted trypanosome development

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue JUL, 2013, Pages

  Geiger, Anne ^a   Fardeau, Marie Laure ^b   Njiokou, Flobert ^c   Ollivier, Bernard ^b  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b STATION MARINE D ENDOUME   (France)

^c UNIVERSITY OF YAOUNDÉ I   (Cameroon)

Author keywords

Bacteriome; Human African trypanosomiasis; Interactions; Trypanosome; Tsetse flies

Indexed keywords

REACTIVE OXYGEN METABOLITE;

AFRICAN TRYPANOSOMIASIS; BACTERIAL FLORA; BACTERIAL TRANSMISSION; BACTERIUM ISOLATION; DISEASE ASSOCIATION; DISEASE TRANSMISSION; DNA FRAGMENTATION; ENVIRONMENTAL FACTOR; GEOGRAPHIC DISTRIBUTION; GLOSSINA; HUMAN; INFECTION RATE; INTESTINE FLORA; MIXED INFECTION; MOLECULAR PHYLOGENY; MORTALITY; NONHUMAN; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PARASITOSIS; PREVALENCE; REVIEW; SPOROZOITE; TRYPANOSOMA; ANIMAL; BACTERIA; BIODIVERSITY; CLASSIFICATION; GASTROINTESTINAL TRACT; GLOSSINIDAE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; PARASITOLOGY; PHYLOGEOGRAPHY; BACTERIOME; BACTERIUM; INTERACTIONS;

ANIMALS; BACTERIA; BIODIVERSITY; GASTROINTESTINAL TRACT; PHYLOGEOGRAPHY; TRYPANOSOMA; TSETSE FLIES;

BACTERIOME; HUMAN AFRICAN TRYPANOSOMIASIS; INTERACTIONS; TRYPANOSOME; TSETSE FLIES;

EID: 84891414140     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2013.00034     Document Type: Review

References (64)

1. Akman, L., Yamashita, A., Watanabe, H., Oshima, K., Shiba, T., Hattori, M., and et al. (2002). Genome sequence of the endocellular obligate symbiont of tsetse, Wigglesworthia glossinidia. Nat. Genet. 32, 402-407. doi: 10.1038/ng986
2. Aksoy, S. (2000). Tsetse-a haven for microorganisms. Parasitol. Today 16, 114-118. doi: 10.1016/S0169-4758(99)01606-3
3. Alam, U., Medlock, J., Brelsfoard, C., Pais, R., Lohs, C., Balmand, S., and et al. (2011). Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the tsetse fly Glossina morsitans. PLoS Pathog. 7:e1002415. doi: 10.1371/journal.ppat.1002415
4. Azambuja, P., Feder, D., and Garcia, E. S. (2004). Isolation of Serratia Marcescens in the midgut of Rhodnius prolixus: impact on the establishment of the parasite Trypanosoma cruzi in the vector. Exp. Parasitol. 107, 89-96. doi: 10.1016/j.exppara.2004.04.007
5. Barrett, M. P. (2006). The rise and fall of sleeping sickness. Lancet 367, 1377-1378. doi: 10.1016/S0140-6736(06)68591-7
6. Beier, M. S., Pumpuni, C. B., Beier, J. C., and Davis, J. R. (1994). Effects of para-aminobenzoic acid, insulin, and gentamycin on Plasmodium falciparum development in anopheline mosquitoes (Diptera: Culicidae). J. Med. Entomol. 31, 561-565.
7. Boissière, A., Tchioffo, M. T., Bachar, D., Abate, L., Marie, A., Nsango, S. E., and et al. (2012). Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog. 8:e1002742. doi: 10.1371/journal.ppat.1002742
8. Broderick, N. A., and Lemaitre, B. (2012). Gut-associated microbes of Drosophila melanogaster. Gut Microbes 3, 307-321. doi: 10.4161/gmic.19896
9. Campbell, C., Mummey, D., Schmidtmann, E., and Wilson, W. (2004). Culture-independent analysis of midgut microbiota in the arbovirus vector Culicoides sonorensis (Diptera: Ceratopogonidae). J. Med. Entomol. 41, 340-348. doi: 10.1603/0022-2585-41.3.340
10. Cattand, P., Jannin, J., and Lucas, P. (2001). Sleeping sickness surveillance: an essential step towards elimination. Trop. Med. Int. Health 6, 348-361. doi: 10.1046/j.1365-3156.2001.00669.x
11. Cirimotich, C. M., Dong, Y., Clayton, A. M., Sandiford, S. L., Souza-Neto, J. A., Mulenga, M., and et al. (2011). Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332, 855-858. doi: 10.1126/science.1201618
12. Coburn, P. S., and Gilmore, M. S. (2003). The Enterococcus faecalis cytolysin: a novel toxin active against eukaryotic and prokaryotic cells. Cell. Microbiol. 5, 661-669. doi: 10.1046/j.1462-5822.2003.00310.x
13. Dale, C., and Maudlin, I. (1999). Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int. J. Syst. Bacteriol. 49, 267-275. doi: 10.1099/00207713-49-1-267
14. de Koning, H. P. (2001). Transporters in African trypanosomes: role in drug action and resistance. Int. J. Parasitol. 31, 512-522. doi: 10.1016/S0020-7519(01)00167-9
15. Díaz-Ruiz, C., Montaner, B., and Pérez-Tomás, R. (2001). Prodigiosin induces cell death in gastric cancer cell line. Histol. Histopathol. 16, 415-421.
16. Dillon, R. J., and Dillon, V. M. (2004). The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 49, 71-92. doi: 10.1146/annurev.ento.49.061802.123416
17. Dong, Y., Manfredini, F., and Dimopoulos, G. (2009). Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 5:e1000423. doi: 10.1371/journal.ppat.1000423
18. Farikou, O., Njiokou, F., Simo, G., Asonganyi, T., Cuny, G., and Geiger, A. (2010). Tsetse fly blood meal modification and trypanosome identification in two sleeping sickness foci in the forest of southern Cameroon. Acta Trop. 116, 81-88. doi: 10.1016/j.actatropica.2010.06.002
19. Fèvre, E. M., Wissmann, B. V., Welburn, S. C., and Lutumba, P. (2008). The burden of human African trypanosomiasis. PLoS Negl. Trop. Dis. 2:e333. doi: 10.1371/journal.pntd.0000333
20. Geiger, A., Fardeau, M. L., Falsen, E., Ollivier, B., and Cuny, G. (2010). Serratia glossinae sp. nov., isolated from the midgut of the tsetse fly Glossina palpalis gambiensis. Int. J. Syst. Evol. Microbiol. 60, 1261-1265. doi: 10.1099/ijs.0.013441-0
21. Geiger, A., Fardeau, M. L., Grebaut, P., Vatunga, G., Josénando, T., Herder, S., and et al. (2009). First isolation of Enterobacter, Enterococcus, and Acinetobacter spp. as inhabitants of the tsetse fly (Glossina palpalis palpalis) midgut. Infect. Genet. Evol. 9, 1364-1370. doi: 10.1016/j.meegid.2009.09.013
22. Geiger, A., Fardeau, M. L., Njiokou, F., Joseph, M., Asonganyi, T., Ollivier, B., and et al. (2011). Bacterial diversity associated with populations of Glossina spp. from Cameroon and distribution within the Campo sleeping sickness focus. Microb. Ecol. 62, 632-643. doi: 10.1007/s00248-011-9830-y
23. Geiger, A., Ravel, S., Mateille, T., Janelle, J., Patrel, D., Cuny, G., and et al. (2007). Vector competence of Glossina palpalis gambiensis for Trypanosoma brucei s.l. and genetic diversity of the symbiont Sodalis glossinidius. Mol. Biol. Evol. 24, 102-109. doi: 10.1093/molbev/msl135
24. Gilboa-Garber, N. (1972). Purification and properties of haemagglutinin from Pseudomonas aeruginosa and its reaction with human blood cells. Biochim. Biophys. Acta 273, 165-173. doi: 10.1016/0304-4165(72)90204-8
25. Gonzalez-Ceron, L., Santillan, F., Rodriguez, M. H., Mendez, D., and Hernandez-Avila, J. E. (2003). Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J. Med. Entomol. 40, 371-374. doi: 10.1603/0022-2585-40.3.371
26. Hammes, W., and Hertel, C. (2006). "The genera Lactobacillus and Carnobacterium," in The Prokaryotes, eds M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (New York, NY: Springer), 320-403. doi: 10.1007/0-387-30744-3_10
27. Hertle, R., Hilger, M., Weingardt-Kocher, S., and Walev, I. (1999). Cytotoxic action of Serratia marcescens hemolysin on human epithelial cells. Infect. Immun. 67, 817-825.
28. Hongoh, Y., Deevong, P., Inoue, T., Moriya, S., Trakulnaleamsai, S., Ohkuma, M., and et al. (2005). Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl. Environ. Microbiol. 71, 6590-6599. doi: 10.1128/AEM.71.11.6590-6599.2005
29. Jackson, T. J., Wang, H. Y., Nugent, M. J., Griffin, C. T., Burnell, A. M., and Dowds, B. C. A. (1995). Isolation of insect pathogenic bacteria, Providencia rettgeri, from Heterorhabditis spp. J. Appl. Bacteriol. 78, 237-244. doi: 10.1111/j.1365-2672.1995.tb05022.x
30. Jeyaprakash, A., Hoy, M. A., and Allsopp, M. H. (2003). Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences. J. Invertebr. Pathol. 84, 96-103. doi: 10.1016/j.jip.2003.08.007
31. Kaaya, G. P., and Darji, N. (1989). Mortality in adult tsetse, Glossina morsitans morsitans, caused by entomopathogenic bacteria. J. Invertebr. Pathol. 54, 32-38. doi: 10.1016/0022-2011(89)90136-5
32. Lacey, L. A. (ed.). (1997). Manual of Techniques in Insect Pathology. San Diego, CA: Academic Press.
33. Lazaro, J. E., Nitcheu, J., Predicala, R. Z., Mangalindan, G. C., Nesslany, F., Marzin, D., and et al. (2002). Heptyl prodigiosin, a bacterial metabolite is antimalarial in vivo and non-mutagenic in vitro. J. Nat. Toxins 11, 367-377.
34. Lindh, J. M., and Lehane, M. J. (2011). The tsetse fly Glossina fuscipes fuscipes (Diptera: Glossina) harbours a surprising diversity of bacteria other than symbionts. Antonie Van Leeuwenhoek 99, 711-720. doi: 10.1007/s10482-010-9546-x
35. Lysyk, T. J., Kalischuk-Tymensen, L., Selinger, L. B., Lancaster, R. C., Wever, L., and Cheng, K. J. (1999). Rearing stable fly larvae (Diptera: Muscidae) on an egg yolk medium. J. Med. Entomol. 36, 382-388.
36. MacLeod, E. T., Maudlin, I., Darby, A. C., and Welburn, S. C. (2007). Antioxidants promote establishment of trypanosome infections in tsetse. Parasitology 134, 827-831. doi: 10.1017/S0031182007002247
37. Maeda, H., and Morihara, K. (1995). Serralysin and related proteinases. Methods Enzymol. 248, 395-413. doi: 10.1016/0076-6879(95)48026-9
38. Maidak, B. L., Cole, J. R., Lilburn, T. G., Parker, C. T. Jr. Saxman, P. R., Farris, R. J., and et al. (2001). The RDP-II (Ribosomal Database Project). Nucleic Acids Res. 29, 173-174.
39. Mercado, T. I., and Colon-Whitt, A. (1982). Lysis of Trypanosoma cruzi by Pseudomonas fluorescens. Antimicrob. Agents Chemother. 22, 1051-1057. doi: 10.1128/AAC.22.6.1051
40. Montaner, B., and Perez-Tomas, R. (2003). The prodigiosins: a new family of anticancer drugs. Curr. Cancer Drug Targets 3, 57-65. doi: 10.2174/1568009033333772
41. Moss, M. (2002). Bacterial pigments. Microbiologist 3, 10-12.
42. O'Neill, S. L., Gooding, R. H., and Aksoy, S. (1993). Phylogenetically distant symbiotic microorganisms reside in Glossina midgut and ovary tissues. Med. Vet. Entomol. 7, 377-383.
43. Poinar, Jr. G. O. Wassink, H. J., Leegwater-van der Linden, M. E., and van der Geest, L. P. (1979). Serratia marcescens as a pathogen of tsetse flies. Acta Trop. 36, 223-227.
44. Pumpuni, C. B., Beier, M. S., Nataro, J. P., Guers, L. D., and Davis, J. R. (1993). Plasmodium falciparum: inhibition of sporogonic development in Anopheles stephensi by gram-negative bacteria. Exp. Parasitol. 77, 195-199. doi: 10.1006/expr.1993.1076
45. Pumpuni, C. B., DeMaio, J., Kent, M., Davis, J. R., and Beier, J. C. (1996). Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am. J. Trop. Med. Hyg. 54, 214-218.
46. Schalk, I. J., Abdallah, M. A., and Pattus, F. (2002). Recycling of pyoverdin on the FpvA receptor after ferric pyoverdin uptake and dissociation in Pseudomonas aeruginosa. Biochemistry 41, 1663-1671. doi: 10.1021/bi0157767
47. Schlein, Y., Polacheck, I., and Yuval, B. (1985). Mycoses, bacterial infections and antibacterial activity in sandflies (Psychodidae) and their possible role in the transmission of leishmaniasis. Parasitology 90, 57-66. doi: 10.1017/S0031182000049015
48. Schmitt-Wagner, D., Friedrich, M. W., Wagner, B., and Brune, A. (2003). Phylogenetic diversity, abundance, and axial distribution of bacteria in the intestinal tract of two soil-feeding termites (Cubitermes spp.). Appl. Environ. Microbiol. 69, 6007-6017. doi: 10.1128/AEM.69.10.6007-6017.2003
49. Simarro, P. P., Diarra, A., Ruiz Postigo, J. A., Franco, J. R., and Jannin, J. G. (2011). The human African trypanosomiasis control and surveillance programme of the World Health Organization 2000-2009: the way forward. PLoS Negl. Trop. Dis. 5:e1007. doi: 10.1371/journal.pntd.0001007
50. Simo, G., Njiokou, F., Mbida Mbida, J. A., Njitchouang, G. R., Herder, S., Asonganyi, T., and et al. (2008). Tsetse fly host preference from sleeping sickness foci in Cameroon: epidemiological implications. Infect. Genet. Evol. 8, 34-39. doi: 10.1016/j.meegid.2007.09.005
51. Steinhaus, E. A. (1960). The importance of environmental factors in the insect-microbe ecosystem. Bacteriol. Rev. 24, 365-373.
52. Straif, S. C., Mbogo, C. N. M., Toure, A. M., Walker, E. D., Kaufman, M., Toure, Y. T., and et al. (1998). Midgut bacteria in Anopheles gambiae and An. funestus (Diptera: Culicidae) from Kenya and Mali. J. Med. Entomol. 35, 222-226.
53. Thomson, N. R., Crow, M. A., McGowan, S. J., Cox, A., and Salmond, G. P. C. (2000). Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control. Mol. Microbiol. 36, 539-556. doi: 10.1046/j.1365-2958.2000.01872.x
54. Van Den Abbeele, J., Claes, Y., Bockstaele, D., Ray, D., and Coosemans, M. (1999). Trypanosoma brucei spp. development in the tsetse fly: characterization of the post-mesocyclic stages in the foregut and proboscis. Parasitology 118, 469-478. doi: 10.1017/S0031182099004217
55. Vickerman, K., Tetley, L., Hendry, A., and Turner, C. M. (1988). Biology of African trypanosomes in the tsetse fly. Biol. Cell. 64, 109-119. doi: 10.1016/0248-4900(88)90070-6
56. Wang, J., Brelsfoard, C., Wu, Y., and Aksoy, S. (2012). Intercommunity effects on microbiome and GpSGHV density regulation in tsetse flies. J. Invertebr. Pathol. 112, S32-S39. doi: 10.1016/j.jip.2012.03.028
57. Wang, J., Wu, Y., Yang, G., and Aksoy, S. (2009). Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc. Natl. Acad. Sci. U.S.A. 106, 12133-12138. doi: 10.1073/pnas.0901226106
58. Weiss, B., and Aksoy, S. (2011). Microbiome influences on insect host vector competence. Trends Parasitol. 27, 514-522. doi: 10.1016/j.pt.2011.05.001
59. Weiss, B. L., Maltz, M., and Aksoy, S. (2012). Obligate symbionts activate immune system development in the tsetse fly. J. Immunol. 188, 3395-3403. doi: 10.4049/jimmunol.1103691
60. Weiss, B. L., Wang, J., and Aksoy, S. (2011). Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol. 9:e1000619. doi: 10.1371/journal.pbio.1000619
61. Weiss, B. L., Wang, J., Maltz, M. A., Wu, Y., and Aksoy, S. (2013). Trypanosome infection establishment in the tsetse fly gut is influenced by microbiome-regulated host immune barriers. PLoS Pathog. 9:e1003318. doi: 10.1371/journal.ppat.1003318
62. Welburn, S. C., and Maudlin, I. (1999). Tsetse-trypanosome interactions: rites of passage. Parasitol. Today 15, 399-403. doi: 10.1016/S0169-4758(99)01512-4
63. Welburn, S. C., Maudlin, I., and Simarro, P. P. (2009). Controlling sleeping sickness - a review. Parasitology 136, 1943-1949. doi: 10.1017/S0031182009006416
64. WHO. (2010). "African trypanosomiasis (sleeping sickness)," in Report of a WHO Expert Committee, 259. Geneva: WHO Technical Report Series.