Mosquito/microbiota interactions: From complex relationships to biotechnological perspectives

Current Opinion in Microbiology

Volumn 15, Issue 3, 2012, Pages 278-284

  Ricci, Irene ^a   Damiani, Claudia ^a   Capone, Aida ^a   DeFreece, Chenoa ^a   Rossi, Paolo ^a   Favia, Guido ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; CECROPIN; DEFENSIN; MYCOTOXIN; POLYPEPTIDE ANTIBIOTIC AGENT; SERINE PROTEINASE;

ACETOBACTER; AEDES; BACTERIAL LOAD; CANDIDA; CULEX; DENGUE; DISEASE CONTROL; DISEASE TRANSMISSION; DROSOPHILA; ENTEROBACTER; ESCHERICHIA; GAMETOCYTE; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE SYSTEM; INNATE IMMUNITY; INSECT; INSECT GENETICS; INTESTINE FLORA; KLEBSIELLA; LACTOBACILLUS PLANTARUM; LARVA; MICROFLORA; MOSQUITO; NONHUMAN; OOCYST; ORGANISMAL INTERACTION; PARTHENOGENESIS; PHAGOCYTOSIS; PICHIA; PLASMODIUM; PROTEIN EXPRESSION; PROTEOBACTERIA; PSEUDOMONADACEAE; PSEUDOMONAS; REVIEW; RICKETTSIACEAE INFECTION; SERRATIA; STAPHYLOCOCCUS; SYMBIONT; SYMBIOSIS; VECTOR CONTROL; WOLBACHIA; YEAST; YELLOW FEVER;

ANIMALS; BIOTECHNOLOGY; CULICIDAE; HOST-PATHOGEN INTERACTIONS; INSECT VECTORS; METAGENOME; WOLBACHIA; YEASTS;

EID: 84864068771     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2012.03.004     Document Type: Review

References (71)

1. Feldhaar H., Gross R. Immune reactions of insects on bacterial pathogens and mutualists. Microbes Infect 2008, 10:1082-1088.
2. Fang J. Ecology: a world without mosquitoes. Nature 2010, 466:432-434.
3. Tolle M.A. Mosquito-borne diseases. Curr Probl Pediatr Adolesc Health Care 2009, 4:97-140.
4. Cirimotich C.M., Dong Y., Clayton A.M., Sandiford S.L., Souza-Neto J.A., Mulenga M., Dimopoulos G. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Nature 2011, 13:855-858.
5. Hertig M., Wolbach S.B. Studies on Rickettsia-like microorganisms in insects. J Med Res 1924, 44:329-374.
6. Werren J.H. Wolbachia run amok. Proc Natl Acad Sci USA 1997, 94:11154-11155.
7. Ricci I., Cancrini G., Gabrielli S., D'Amelio S., Favia G. Searching for Wolbachia (Rickettsiales: Rickettsiaceae) in mosquitoes (Diptera: Culicidae): large polymerase chain reaction survey and new identifications. J Med Entomol 2002, 39:562-567.
8. Kittayapong P., Baisley K.J., Baimai V., O'Neill S.L. Distribution and diversity of Wolbachia infections in Southeast Asian mosquitoes (Diptera: Culicidae). J Med Entomol 2000, 37:340-345.
9. Dean J.L., Dobson S.L. Characterization of Wolbachia infections and interspecific crosses of Aedes (Stegomyia) polynesiensis and Ae. (Stegomyia) riversi (Diptera: Culicidae). J Med Entomol 2004, 41:894-900.
10. Tsai K.H., Huang C.G., Wu W.J., Chuang C.K., Lin C.C., Chen W.J. Parallel infection of Japanese encephalitis virus and Wolbachia within cells of mosquito salivary glands. J Med Entomol 2006, 43:752-756.
11. The malERA Consultative Group on Vector Control A research agenda for malaria eradication: vector control. PLoS Med 2011, 8:e1000401.
12. Service M.W. Importance of ecology in Aedes aegypti control. Southeast Asian J Trop Med Public Health 1992, 23:681-690.
13. Yen J.H., Barr A.R. New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 1971, 232:657-658.
14. Stouthamer R., Breeuwer J.A., Hurst G.D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 1999, 53:71-102.
15. Rousset F., Bouchon D., Pintureau B., Juchault P., Solignac M. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc Biol Sci 1992, 250:91-98.
16. Hurst G.D., Johnson A.P., Schulenburg J.H., Fuyama Y. Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 2000, 156:699-709.
17. Sinkins S.P. Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem Mol Biol 2004, 34:723-729.
18. McMeniman C.J., Lane R.V., Cass B.N., Fong A.W., Sidhu M., Wang Y.F., O'Neill S.L. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 2009, 323:141-144.
19. Kambris Z., Cook P.E., Phuc H.K., Sinkins S.P. Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 2009, 326:134-136.
20. 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., et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell Dec 2009, 139:1268-1278.
21. Kambris Z., Blagborough A.M., Pinto S.B., Blagrove M.S., Godfray H.C., Sinden R.E., Sinkins S.P. Wolbachia stimulates immune gene expression and inhibits Plasmodium development in Anopheles gambiae. PLoS Pathog 2010, 6:e1001143.
22. Hughes G.L., Vega-Rodriguez J., Xue P., Rasgon J.L. Wolbachia strain wAlbB enhances infection by the rodent malaria parasite Plasmodium berghei in Anopheles gambiae mosquitoes. Appl Environ Microbiol 2011, 78:1491-1495.
23. Hoffmann A.A., Montgomery B.L., Popovici J., Iturbe-Ormaetxe I., Johnson P.H., Muzzi F., Greenfield M., Durkan M., Leong Y.S., Dong Y., et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 2011, 474:454-457.
24. Rasgon J.L. Dengue fever: mosquitoes attacked from within. Nature 2011, 476:407-408.
25. Pidiyar V., Kaznowski A., Narayan N.B., Patole M., Shouche Y.S. Aeromonas culicicola sp. nov., from the midgut of Culex quinquefasciatus. Int J Syst Evol Microbiol 2002, 52:1723-1728.
26. Pidiyar V.J., Jangid K., Patole M.S., Shouche Y.S. Studies on cultured and uncultured microbiota of wild Culex quinquefasciatus mosquito midgut based on 16s ribosomal RNA gene analysis. Am J Trop Med Hyg 2004, 70:597-603.
27. Touré A.M., Mackey A.J., Wang Z.X., Beier J.C. Bactericidal effects of sugar-fed antibiotics on resident midgut bacteria of newly emerged anopheline mosquitoes (Diptera: Culicidae). J Med Entomol 2000, 37:246-249.
28. Demaio J., Pumpuni C.B., Kent M., Beier J.C. The midgut bacterial flora of wild Aedes triseriatus, Culex pipiens, and Psorophora columbiae mosquitoes. Am J Trop Med Hyg 1996, 54:219-223.
29. Douglas A.E., Smith D.C. Are endosymbioses mutualistic?. Trends Ecol Evol 1989, 4:350-352.
30. Gusmão D.S., Santos A.V., Marini D.C., Bacci M., Berbert-Molina M.A., Lemos F.J. Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Trop 2010, 115:275-281.
31. Wang Y., Gilbreath T.M., Kukutla P., Yan G., Xu J. Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS ONE 2011, 6:e24767.
32. Fouda M.A., Hassan M.I., Al-Daly A.G., Hammad K.M. Effect of midgut bacteria of Culex pipiens L. on digestion and reproduction. J Egypt Soc Parasitol 2001, 31:767-780.
33. 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.
34. Xi Z., Ramirez J.L., Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 2008, 4:e1000098.
35. Weiss B., Aksoy S. Microbiome influences on insect host vector competence. Trends Parasitol 2011, 27:514-522.
36. Cirimotich C.M., Dong Y., Garver L.S., Sim S., Dimopoulos G. Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol 2010, 34:387-395.
37. 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.
38. Dong Y., Manfredini F., Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 2009, 5:e1000423.
39. Marquardt W.C., Kondratieff B.C. Biology of Disease Vectors 2005, Elsevier Academic Press. edn 2.
40. Dimopoulos G. Insect immunity and its implication in mosquito-malaria interactions. Cell Microbiol 2003, 5:3-14.
41. Gross T.L., Myles K.M., Adelman Z.N. Identification and characterization of heat shock 70 genes in Aedes aegypti (Diptera: Culicidae). J Med Entomol 2009, 46:496-504.
42. Meister S., Agianian B., Turlure F., Relógio A., Morlais I., Kafatos F.C., Christophides G.K. Anopheles gambiae PGRPLC-mediated defense against bacteria modulates infections with malaria parasites. PLoS Pathog 2009, 8:e1000542.
43. Riehle M.A., Jacobs-Lorena M. Using bacteria to express and display anti-parasite molecules in mosquitoes: current and future strategies. Insect Biochem Mol Biol 2005, 35:699-707.
44. Beier M.S., Pumpuni C.B., Beier J.C., Davis J.R. Effects of para-aminobenzoic acid, insulin, and gentamicin on Plasmodium falciparum development in anopheline mosquitoes (Diptera: Culicidae). J Med Entomol 1994, 31:561-565.
45. Kämpfer P., Terenius O., Lindh J.M., Faye I. Janibacter anophelis sp. nov., isolated from the midgut of Anopheles arabiensis. Int J Syst Evol Microbiol 2006, 56:389-392.
46. Lindh J.M., Borg-Karlson A.K., Faye I. Trans stadial and horizontal transfer of bacteria within a colony of Anopheles gambiae (Diptera: Culicidae) and oviposition response to bacteria-containing water. Acta Trop 2008, 107:242-250.
47. Kämpfer P., Matthews H., Glaeser S.P., Martin K., Lodders N., Faye I. Elizabethkingia anophelis sp. nov., isolated from the midgut of the mosquito Anopheles gambiae. Int J Syst Evol Microbiol 2011, 61:2670-2675.
48. Favia G., Ricci I., Damiani C., Raddadi N., Crotti E., Marzorati M., Rizzi A., Urso R., Brusetti L., Borin S., et al. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proc Natl Acad Sci USA 2007, 104:9047-9051.
49. Favia G., Ricci I., Marzorati M., Negri I., Alma A., Sacchi L., Bandi C., Daffonchio D. Bacteria of the genus Asaia: a potential paratransgenic weapon against malaria. Adv Exp Med Biol 2008, 627:49-59.
50. Damiani C., Ricci I., Crotti E., Rossi P., Rizzi A., Scuppa P., Capone A., Ulissi U., Epis S., Genchi M., et al. Mosquito-bacteria symbiosis: the case of Anopheles gambiae and Asaia. Microb Ecol 2010, 60:644-654.
51. Crotti E., Damiani C., Pajoro M., Gonella E., Rizzi A., Ricci I., Negri I., Scuppa P., Rossi P., Ballarini P., et al. Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ Microbiol 2009, 11:3252-3264.
52. Damiani C., Ricci I., Crotti E., Rossi P., Rizzi A., Scuppa P., Esposito F., Bandi C., Daffonchio D., Favia G. Paternal transmission of symbiotic bacteria in malaria vectors. Curr Biol 2008, 18:1087-1088.
53. Chouaia B., Rossi P., Epis S., Mosca M., Ricci I., Damiani C., Ulissi U., Crotti E., Daffonchio D., Bandi C., Favia G. Delayed larval development in Anopheles mosquitoes deprived of Asaia bacterial symbionts. BMC Microbiol 2012, 12. Suppl 1:S2 [Epub ahead of print].
54. Shin S.C., Kim S.H., You H., Kim B., Kim A.C., Lee K.A., Yoon J.H., Ryu J.H., Lee W.J. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 2011, 334:670-674.
55. Storelli G., Defaye A., Erkosar B., Hols P., Royet J., Leulier F. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 2011, 14:403-414.
56. Gusmão D.S., Santos A.V., Marini D.C., Russo Ede S., Peixoto A.M., Bacci Júnior M., Berbert-Molina M.A., Lemos F.J. First isolation of microorganisms from the gut diverticulum of Aedes aegypti (Diptera: Culicidae): new perspectives for an insect-bacteria association. Mem Inst Oswaldo Cruz 2007, 102:919-924.
57. Ignatova E.A., Nagornaia S.S., Povazhnaia T.N., Ianishevskaia G.S. The yeast flora of blood-sucking mosquitoes. Mikrobiol Z 1996, 58:12-15.
58. Ricci I., Mosca M., Valzano M., Damiani C., Scuppa P., Rossi P., Crotti E., Cappelli A., Ulissi U., Capone A., et al. Different mosquito species host Wickerhamomyces anomalus (Pichia anomala): perspectives on vector-borne diseases symbiotic control. Antonie Van Leeuwenhoek 2011, 99:43-50.
59. Ricci I., Damiani C., Scuppa P., Mosca M., Crotti E., Rossi P., Rizzi A., Capone A., Gonella E., Ballarini P., et al. The yeast Wickerhamomyces anomalus (Pichia anomala) inhabits the midgut and reproductive system of the Asian malaria vector Anopheles stephensi. Environ Microbiol 2011, 13:911-921.
60. Wang X., Chi Z., Yue L., Li J., Li M., Wu L. A marine killer yeast against the pathogenic yeast strain in crab (Portunus trituberculatus) and an optimization of the toxin production. Microbiol Res 2007, 62:77-85.
61. Wang L., Yue L., Chi Z., Wang X. Marine killer yeasts active against a yeast strain pathogenic to crab Portunus trituberculatus. Dis Aquat Organ 2008, 80:211-218.
62. Fredlund E., Druvefors U., Boysen M.E., Lingsten K.J., Schnürer J. Physiological characteristics of the biocontrol yeast Pichia anomala J121. FEMS Yeast Res 2002, 2:395-402.
63. Séguy N., Polonelli L., Dei-Cas E., Cailliez J.C. Effect of a killer toxin of Pichia anomala to Pneumocystis. Perspectives in the control of pneumocystosis. FEMS Immunol Med Microbiol 1998, 22:145-149.
64. Magliani W., Conti S., Arseni S., Frazzi R., Salati A., Polonelli L. Killer anti-idiotypes in the control of fungal infections. Curr Opin Investig Drugs 2001, 2:477-479.
65. Savoia D., Avanzini C., Conti S., Magliani V., Frazzi R., Polonelli L. In vitro leishmanicidal activity of a monoclonal antibody mimicking a yeast killer toxin. J Eukaryot Microbiol 2002, 49:319-323.
66. Gaio Ade O., Gusmão D.S., Santos A.V., Berbert-Molina M.A., Pimenta P.F., Lemos F.J. Contribution of midgut bacteria to blood digestion and egg production in Aedes aegypti (Diptera: Culicidae) (L.). Parasit Vectors 2011, 4:105.
67. Beard C.B., Dotson E.M., Pennington P.M., Eichler S., Cordon-Rosales C., Durvasula R.V. Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease. Int J Parasitol 2001, 31:621-627.
68. Bisi D.C., Lampe D.J. Secretion of anti-Plasmodium effector proteins from a natural Pantoea agglomerans isolate by using PelB and HlyA secretion signals. Appl Environ Microbiol 2011, 77:4669-4675.
69. Patil CD, Patil SV, Salunke BK, Salunkhe RB: Insecticidal potency of bacterial species Bacillus thuringiensis SV2 and Serratia nematodiphila SV6 against larvae of mosquito species Aedes aegypti, Anopheles stephensi, and Culex quinquefasciatus. Parasitol Res 2011, in press. [Epub ahead of print].
70. Ren X., Hoiczyk E., Rasgon J.L. Viral paratransgenesis in the malaria vector Anopheles gambiae. PLoS Pathog 2008, 4:e1000135.
71. Fang W., Vega-Rodríguez J., Ghosh A.K., Jacobs-Lorena M., Kang A., St Leger R.J. Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science 2011, 331:1074-1077.