Mosquitoes rely on their gut microbiota for development

Molecular Ecology

Volumn 23, Issue 11, 2014, Pages 2727-2739

  Coon, Kerri L ^a   Vogel, Kevin J ^a   Brown, Mark R ^a   Strand, Michael R ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

bacteria; development; evolution; insects; microbial biology

Indexed keywords

AEDES AEGYPTI; ANOPHELES GAMBIAE; BACTERIA (MICROORGANISMS); CULICIDAE; ESCHERICHIA COLI; HEXAPODA;

BACTERIAL DNA; RNA 16S;

ANIMAL; ARTICLE; BACTERIUM; CLASSIFICATION; DEVELOPMENT; EVOLUTION; FEMALE; GASTROINTESTINAL TRACT; GENETICS; GERMFREE ANIMAL; INSECT; LARVA; MICROBIAL BIOLOGY; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS; MOSQUITO; NUCLEOTIDE SEQUENCE; OOCYTE; SPECIES DIFFERENCE;

BACTERIA; DEVELOPMENT; EVOLUTION; INSECTS; MICROBIAL BIOLOGY;

ANIMALS; BACTERIA; CULICIDAE; DNA, BACTERIAL; FEMALE; GASTROINTESTINAL TRACT; GERM-FREE LIFE; LARVA; MICROBIOTA; MOLECULAR SEQUENCE DATA; OVUM; RNA, RIBOSOMAL, 16S; SPECIES SPECIFICITY;

EID: 84901478997     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12771     Document Type: Article

References (60)

1. Bahia AC, Dong Y, Blumberg BJ, et al,. (2014) Exploring Anopheles gut bacteria for Plasmodium blocking activity. Environmental Microbiology, doi: 10.1111/1462-2920.12381.
2. Beck M, Strand MR, (2003) RNA interference silences Microplitis demolitor bracovirus genes and implicates glc1.8 in disruption of adhesion in infected host cells. Virology, 314, 521-535.
3. Boissiere A, Tchioffo MT, Bachar D, et al,. (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathogens, 8, e1002742.
4. Briegel H, (2003) Physiological bases of mosquito ecology. Journal of Vector Ecology, 28, 1-11.
5. Briones AM, Shililu J, Githure J, Novak R, Raskin L, (2008) Thorsellia anophelis is the dominant bacterium in a Kenyan population of adult Anopheles gambiae mosquitoes. ISME Journal, 2, 74-82.
6. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R, (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics, 26, 266-267.
7. Caporaso JG, Kuczynski J, Stombaugh J, et al,. (2010b) QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335-336.
8. Chao J, Wistreich GA, Moore J, (1963) Failure to isolate microorganisms from within mosquito eggs. Annals of the Entomological Society of America, 56, 559-561.
9. Chavshin AR, Oshaghi MA, Vatandoost H, et al,. (2012) Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: a step toward finding suitable paratransgenesis candidates. Acta Tropica, 121, 129-134.
10. Chouaia B, Rossi P, Montagna M, et al,. (2010) Molecular evidence for multiple infections as revealed by typing of Asaia bacterial symbionts of four mosquito species. Applied Environmental Microbiology, 76, 7444-7450.
11. Chouaia B, Rossi P, Epis S, et al,. (2012) Delayed larval development in Anopheles mosquitoes deprived of Asaia bacterial symbionts. BMC Microbiology, 12, S2.
12. Cirimotich CM, Dong YM, Clayton AM, et al,. (2011) Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science, 332, 855-858.
13. Clements AN, (1992) The Biology of Mosquitoes, Vol. 1. Development, Nutrition, and Reproduction. Chapman & Hall, New York.
14. Cole JR, Wang Q, Cardenas E, et al,. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research, 37, D141-D145.
15. Corby-Harris V, Pontaroli AC, Shimkets LJ, Bennetzen JL, Habel KE, Promislow DEL, (2007) Geographical distribution and diversity of bacteria associated with natural populations of Drosophila melanogaster. Applied Environmental Microbiology, 73, 3470-3479.
16. Damiani C, Ricci I, Crotti E, et al,. (2010) Mosquito-bacteria symbiosis: the case of Anopheles gambiae and Asaia. Microbial Ecology, 60, 644-654.
17. DeMaio J, Pumpuni CB, Kent M, Beier JC, (1996) The midgut bacterial flora of wild Aedes triseriatus, Culex pipiens, and Psorophora columbiae mosquitoes. The American Journal of Tropical Medicine and Hygiene, 54, 219-223.
18. DeSantis TZ, Hugenholtz P, Larsen N, et al,. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied Environmental Microbiology, 72, 5069-5072.
19. Djadid ND, Jazayeri H, Raz A, Favia G, Ricci I, Zakeri S, (2011) Identification of the midgut microbiota of An. stephensi and An. maculipennis for their application as a paratransgenic tool against malaria. PLoS ONE, 6, e28484.
20. Dong YM, Manfredini F, Dimopoulos G, (2009) Implication of the mosquito midgut microbiota in defense against malaria parasites. PLoS Pathogens, 5, 1000423.
21. Edgar RC, (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460-2461.
22. Engel P, Moran NA, (2013) The gut microbiota of insects-diversity in structure and function. FEMS Microbiology Reviews, 37, 699-735.
23. Engel P, Martinson VG, Moran NA, (2012) Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences USA, 109, 11002-11007.
24. Favia G, Ricci I, Damiani C, et al,. (2007) Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. Proceedings of the National Academy of Sciences USA, 104, 9047-9051.
25. Foster WA, (1995) Mosquito sugar feeding and reproductive energetics. Annual Review of Entomology, 40, 443-474.
26. Gaio AD, Gusmão DS, Santos AV, Berbert-Molina MA, Pimenta PFP, Lemos FJA, (2011) Contribution of midgut bacteria to blood digestion and egg production in Aedes aegypti (Diptera: Culicidae) (L.). Parasites & Vectors, 4, 105.
27. Gulia-Nuss M, Eum JH, Strand MR, Brown MR, (2012) Ovary ecdysteroidogenic hormone activates egg maturation in the mosquito Georgecraigius atropalpus after adult eclosion or a blood meal. Journal of Experimental Biology, 215, 3758-3767.
28. Gusmão DS, Santos AV, Marini DC, Bacci M, Berbert-Molina MA, Lemos FJA, (2010) Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. Acta Tropica, 115, 275-281.
29. Haas BJ, Gevers D, Earl AM, et al,. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21, 494-504.
30. Katoh K, Kuma K, Toh H, Miyata T, (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511-518.
31. Kittayapong P, Baisley KJ, Baimai V, O'Neill SL, (2000) Distribution and diversity of Wolbachia infections in southeast Asian mosquitoes (Diptera: Culicidae). Journal of Medical Entomology, 37, 340-345.
32. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P, (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environmental Microbiology, 12, 118-123.
33. Lee WJ, Brey PT, (2013) How microbiomes influence metazoan development: insights from history and Drosophila modeling of gut-microbe interactions. Annual Review of Cell Biology, 29, 571-592.
34. Lindh JM, Borg-Karlson A-K, Faye I, (2008) Transstadial and horizontal transfer of bacteria within a colony of Anopheles gambiae (Diptera: Culicidae) and oviposition response to bacteria-containing water. Acta Tropica, 107, 242-250.
35. Lozupone C, Knight R, (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Applied Environmental Microbiology, 71, 8228-8235.
36. Lozupone CA, Hamady M, Kelley ST, Knight R, (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Applied Environmental Microbiology, 73, 1576-1585.
37. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA, (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology, 20, 619-628.
38. McDonald D, Price MN, Goodrich J, et al,. (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME Journal, 6, 610-618.
39. McMeniman CJ, Lane RV, Cass BN, et al,. (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science, 323, 141-144.
40. Merritt RW, Dadd RH, Walker ED, (1992) Feeding behavior, natural food, and nutritional relationships of larval mosquitoes. Annual Review of Entomology, 37, 349-376.
41. Moll RM, Romoser WS, Modrzakowski MC, Moncayo AC, Lerdthusnee K, (2001) Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. Journal of Medical Entomology, 38, 29-32.
42. Moran NA, (2006) Symbiosis. Current Biology, 16, R866-R871.
43. Oliveira JHM, Goncalves RLS, Lara FA, et al,. (2011) Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathogens, 7, 1001320.
44. Osei-Poku J, Mbogo CM, Palmer WJ, Jiggins FM, (2012) Deep sequencing reveals extensive variation in the gut microbiota of wild mosquitoes from Kenya. Molecular Ecology, 21, 5138-5150.
45. Price MN, Dehal PS, Arkin AP, (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE, 5, e9490.
46. Pumpuni CB, Demaio J, Kent M, Davis JR, Beier JC, (1996) Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. American Journal of Tropical Medicine and Hygiene, 54, 214-218.
47. Reidenbach KR, Cook S, Bertone MA, Harbach RE, Wiegmann BM, Besansky NJ, (2009) Phylogenetic analysis and temporal diversification of mosquitoes (Diptera: Culicidae) based on nuclear genes and morphology. BMC Evolutionary Biology, 9, 298.
48. Riehle MA, Brown MR, (2002) Insulin receptor expression during development and a reproductive cycle in the ovary of the mosquito Aedes aegypti. Cell & Tissue Research, 308, 409-420.
49. Sanders JG, Powell S, Kronauer DJC, Vasconcelos HL, Frederickson ME, Pierce NE, (2014) Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Molecular Ecology, 23, 1268-1283.
50. Shin SC, Kim SH, You H, et al,. (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science, 334, 670-674.
51. Staubach F, Baines JF, Kunzel S, Bik EM, Petrov DA, (2013) Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS ONE, 8, e70749.
52. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F, (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metabolism, 14, 403-414.
53. Terenius O, Lindh JM, Eriksson-Gonzales K, et al,. (2012) Midgut bacterial dynamics in Aedes aegypti. FEMS Microbial Ecology, 80, 556-565.
54. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied Environmental Microbiology, 73, 5261-5267.
55. Wang Y, Gilbreath TM, Kukutla P, Yan GY, Xu JN, (2011) Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya. PLoS ONE, 6, e24767.
56. Wong ACN, Ng P, Douglas AE, (2011) Low diversity bacterial community in the gut of the fruitfly Drosophila melanogaster. Environmental Microbiology, 13, 1889-1900.
57. Wotton RS, Chaloner DT, Yardley CA, Merritt RW, (1997) Growth of Anopheles mosquito larvae on dietary microbiota in aquatic surface microlayers. Medical & Veterinary Entomology, 11, 65-70.
58. Xi Z, Ramirez JL, Dimopoulos G, (2008) The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathogens, 4, e1000098.
59. Ye YXH, Woolfit M, Huttley GA, et al,. (2013) Infection with a virulent strain of Wolbachia disrupts genome wide-patterns of cytosine methylation in the mosquito Aedes aegypti. PLoS ONE, 8, e66482.
60. Zhang GM, Hussain M, O'Neill SL, Asgari S, (2013) Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proceedings of the National Academy of Sciences USA, 110, 10276-10281.