Dynamics of midgut microflora and dengue virus impact on life history traits in Aedes aegypti

Acta Tropica

Volumn 140, Issue , 2014, Pages 151-157

  Hill, Casey L ^a   Sharma, Avinash ^b   Shouche, Yogesh ^b   Severson, David W ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b NATIONAL CENTRE FOR CELL SCIENCE   (India)

Author keywords

Aedes aegypti; Dengue; Fitness; Life history trait; Midgut microflora; Vector competence

Indexed keywords

ANTIBIOTIC AGENT;

DENGUE FEVER; DISEASE CONTROL; DISEASE TRANSMISSION; DISEASE VECTOR; FECUNDITY; FITNESS; FLORA; LIFE HISTORY TRAIT; MORBIDITY; MORTALITY; PATHOGEN; VIRAL DISEASE;

ADULT; AEDES AEGYPTI; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CLEARANCE; CONTROLLED STUDY; DENGUE; DENGUE VIRUS; DISEASE CARRIER; FEMALE; FERTILITY; FITNESS; INFECTION RATE; LIFE HISTORY TRAIT; MICROFLORA; MIDGUT; NONHUMAN; SURVIVAL; VIRUS STRAIN; AEDES; ANIMAL; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOSQUITO; SHEEP; TRANSMISSION; VIROLOGY;

AEDES AEGYPTI; DENGUE VIRUS;

AEDES; ANIMALS; DENGUE; DENGUE VIRUS; FEMALE; GASTROINTESTINAL TRACT; INSECT VECTORS; MOSQUITO CONTROL; SHEEP;

EID: 84908454505     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2014.07.015     Document Type: Article

References (45)

1. Apte-Deshpande A., Paingankar M., Gokhale M.D., Deobagkar D.N. Serratia odorifera a midgut inhabitant of Aedes aegypti mosquito enhances its susceptibility to dengue-2 virus. PLoS ONE 2012, 7:e40401.
2. Behura S.K., Gomez-Machorro C., Harker B.W., deBruyn B., Lovin D.D. Global cross-talk of genes of the mosquito Aedes aegypti in response to dengue virus infection. PLoS Negl. Trop. Dis. 2011, 5:e1385.
3. Bennett K.E., Beaty B.J., Black W.C. Selection of D2S3, an A. aegypti (Diptera: Culicidae) strain with high oral susceptibility to Dengue 2 virus and D2MEB, a strain with a midgut barrier to Dengue 2 escape. J. Med. Entomol. 2005, 42:110-119.
4. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., Drake J.M., Brownstein J.S., Hoen A.G., Sankoh O., Myers M.F., George D.B., Jaenisch T., Wint G.R., Simmons C.P., Scott T.W., Farrar J.J., Hay S.I. The global distribution and burden of dengue. Nature 2013, 496:504-507.
5. Blair C.D., Adelman Z.N., Olson K.E. Molecular strategies for interrupting arthropod-borne virus transmission by mosquitoes. Clin. Microbiol. Rev. 2000, 13:651-661.
6. Chadee D.D., Rahaman A. Use of water drums by humans and Aedes aegypti in Trinidad. J. Vector Ecol. 2000, 25:28-35.
7. Charan S.S., Pawar K.D., Severson D.W., Patole M.S., Shouche Y.S. Comparative analysis of midgut bacterial communities of Aedes aegypti mosquito strains varying in vector competence to dengue virus. Parasitol. Res. 2013, 112:2627-2637.
8. Chauhan C., Behura S.K., Debruyn B., Lovin D.D., Harker B.W., Gomez-Machorro C., Mori A., Romero-Severson J., Severson D.W. Comparative expression profiles of midgut genes in dengue virus refractory and susceptible Aedes aegypti across critical period for virus infection. PLoS ONE 2012, 7:e47350.
9. Cirimotich C.M., Dong Y., Garver L.S., Dimopoulos G. Mosquito immune defenses against Plasmodium infection. Dev. Comp. Immunol. 2010, 34:387-395.
10. 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. Science 2011, 332:855-858.
11. Clemons A., Mori A., Haugen M., Severson D.W., Duman-Scheel M. Culturing and egg collection of Aedes aegypti. Cold Spring Harb. Protoc. 2010, 10, pdb.prot5507.
12. Coutinho-Abreu I.V., Zhu K.Y., Ramalho-Ortigao M. Transgenesis and paratransgenesis to control insect-borne diseases: current status and future challenges. Parasitol. Int. 2010, 59:1-8.
13. Dethlefsen L., McFall-Ngai M., Relman D.A. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 2007, 449:811-818.
14. Dillon R.J., Dillon V.M. The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 2004, 49:71-92.
15. Dong Y., Manfredini F., Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 2009, 5:e1000423.
16. Douglas A.E. The Symbiotic Habit 2010, Princeton University Press, Princeton, NJ.
17. 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, 3:767-780.
18. Gaines P.J., Olson K.E., Higgs S., Powers A.M., Beaty B.J., Blair C.D. Pathogen-derived resistance to dengue type 2 virus in mosquito cells by expression of the premembrane coding region of the viral genome. J. Virol. 1996, 70:2132-2137.
19. Gaio A., Gusmao D.S., Santos A.V., Berbert-Molina M.A., Pimenta P., Lemos F. Contribution of midgut bacteria to blood digestion and egg production in Aedes aegypti (Diptera: Culicidae). Parasites Vectors 2011, 4:105.
20. Ley R.E., Lozupone C.A., Hamady M., Knight R., Gordon J.I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 2008, 6:776-788.
21. Maciel-de-Freitas R., Koella J.C., Lourenço-de-Oliveira R. Lower survival rate, longevity and fecundity of Aedes aegypti (Diptera: Culicidae) females orally challenged with dengue virus serotype 2. Trans. R. Soc. Trop. Med. Hyg. 2011, 105:452-458.
22. Maciel-de-Freitas R., Sylvestre G., Gandini M., Koella J.C. The influence of dengue virus serotype-2 infection on Aedes aegypti (Diptera: Culicidae) motivation and avidity to blood feed. PLOS ONE 2013, 8:e65252.
23. Mahmood F., Reisen W.K., Chiles R.E., Fang Y. Western equine encephalomyelitis virus infection affects the life table characteristics of Culex tarsalis (Diptera: Culicidae). J. Med. Entomol. 2004, 41:982-986.
24. 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.
25. Mourya D.T., Gokhale M.D., Pidiyar V., Barde P.V., Patole M., Mishra A.C., Shouche Y. Study of the effect of the midgut bacterial flora of Culex quinquefasciatus on the susceptibility of mosquitoes to Japanese encephalitis virus. Acta Virol. 2002, 46:257-260.
26. Na'was T.E., Hollis D.G., Moss C.W., Weaver R.E. Comparison of biochemical, morphologic, and chemical characteristics of Centers for Disease Control fermentative coryneform groups 1, 2 and A-4. J. Clin. Microbiol. 1987, 25:1354-1358.
27. Nene V., Wortman J.R., Lawson D., Haas B., Kodira C., Tu Z.J., Loftus B., Xi Z., Megy K., Grabherr M., Ren Q., Zdobnov E.M., Lobo N.F., Campbell K.S., Brown S.E., Bonaldo M.F., Zhu J., Sinkins S.P., Hogenkamp D.G., Amedeo P., Arensburger P., Atkinson P.W., Bidwell S., Biedler J., Birney E., Bruggner R.V., Costas J., Coy M.R., Crabtree J., Crawford M., Debruyn B., Decaprio D., Eiglmeier K., Eisenstadt E., El-Dorry H., Gelbart W.M., Gomes S.L., Hammond M., Hannick L.I., Hogan J.R., Holmes M.H., Jaffe D., Johnston J.S., Kennedy R.C., Koo H., Kravitz S., Kriventseva E.V., Kulp D., Labutti K., Lee E., Li S., Lovin D.D., Mao C., Mauceli E., Menck C.F., Miller J.R., Montgomery P., Mori A., Nascimento A.L., Naveira H.F., Nusbaum C., O'leary S., Orvis J., Pertea M., Quesneville H., Reidenbach K.R., Rogers Y.H., Roth C.W., Schneider J.R., Schatz M., Shumway M., Stanke M., Stinson E.O., Tubio J.M., Vanzee J.P., Verjovski-Almeida S., Werner D., White O., Wyder S., Zeng Q., Zhao Q., Zhao Y., Hill C.A., Raikhel A.S., Soares M.B., Knudson D.L., Lee N.H., Galagan J., Salzberg S.L., Paulsen I.T., Dimopoulos G., Collins F.H., Birren B., Fraser-Liggett C.M., Severson D.W. Genome sequence of Aedes aegypti, a major arbovirus vector. Science 2007, 316:1718-1723.
28. Nogge G. Sterility in tsetse flies (Glossina morsitans Westwood) caused by loss of symbionts. Experientia 1976, 32:995-996.
29. 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.
30. 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. Amat. J. Trop. Med. Hyg. 1996, 54:214-218.
31. Ramirez J.L., Souza-Neto J., Cosme R.T., Rovira J., Ortiz A., Pascale J.M., Dimopoulos G. Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLoS Negl. Trop. Dis. 2012, 6:e1561.
32. Rodrigues J., Brayner F.A., Alves L.C., Dixit R., Barillas-Mury C. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010, 329:1353-1355.
33. Rutledge J.C., Ward R.A., Gould D.J. Studies on the feeding response of mosquitoes to nutritive solutions in a new membrane feeder. Mosq. News 1964, 24:407-419.
34. Scott T.W., Naksathit A., Day J.F., Kittayapong P., Edman J.D. A fitness advantage for Aedes aegypti and the viruses it transmits when females feed only on human blood. Am. J. Trop. Med. Hyg. 1997, 57:235-239.
35. Sharma A., Dhayal D., Singh O.P., Adak T., Bhatnagar R.K. Gut microbes influence fitness and malaria transmission potential of Asian malaria vector Anopheles stephensi. Acta Trop. 2013, 128:41-47.
36. Schneider J.R., Mori A., Romero-Severson J., Chadee D.D., Severson D.W. Investigations of dengue-2 susceptibility and body size among Aedes aegypti populations. Med. Vet. Entomol. 2007, 21:370-376.
37. Sessions O.M., Barrows N.J., Souza-Neto J.A., Robinson T.J., Hershey C.L., Rodgers M.A., Ramirez J.L., Dimopoulos G., Yang P.L., Pearson J.L. Discovery of insect and human dengue virus host factors. Nature 2009, 458:1047-1050.
38. Styer L.M., Meola M.A., Kramer L.D. West Nile virus infection decreases fecundity of Culex tarsalis females. J. Med. Entomol. 2007, 44:1074-1085.
39. Terenius O., Lindh J.M., Eriksson-Gonzales K., Bussiere L., Laugen A.T., Bergquist H., Titanji K., Faye I. Midgut bacterial dynamics in Aedes aegypti. FEMS Microbiol. Ecol. 2012, 80:556-565.
40. Thathy V., Severson D.W., Christensen B.M. Reinterpretation of the genetics of susceptibility of Aedes aegypti to Plasmodium gallinaceum. J. Parasitol. 1994, 80:705-712.
41. 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.
42. Vézilier J., Nicot A., Gandon S., Rivero A. Plasmodium infection decreases fecundity and increases survival of mosquitoes. Proc. R. Soc. Biol. Sci. 2012, 279:4033-4041.
43. Xi Z., Ramirez J.L., Dimopoulos G. The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog. 2008, 4:e1000098.
44. Yan G., Severson D.W., Christensen B.M. Costs and benefits of mosquito refractoriness to malaria parasites. Evolution 1997, 51:441-450.
45. Ye Y.H., Woolfit M., Rances E., O'Neill S.L., McGraw E.A. Wolbachia-associated bacterial protection in the mosquito Aedes aegypti. PLoS Negl. Trop. Dis. 2014, 7:e2362.