Skip to main content
SpringerLink
Log in

Competition for Amino Acids Between Wolbachia and the Mosquito Host, Aedes aegypti

  • Invertebrate Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The endosymbiont Wolbachia represents a promising method of dengue control, as it reduces the ability of the primary vector, the mosquito Aedes aegypti, to transmit viruses. When mosquitoes infected with the virulent Wolbachia strain wMelPop are fed non-human blood, there is a drastic reduction in mosquito fecundity and egg viability. Wolbachia has a reduced genome and is clearly dependent on its host for a wide range of nutritional needs. The fitness defects seen in wMelPop-infected A. aegypti could be explained by competition between the mosquito and the symbiont for essential blood meal nutrients, the profiles of which are suboptimal in non-human blood. Here, we examine cholesterol and amino acids as candidate molecules for competition, as they have critical roles in egg structural development and are known to vary between blood sources. We found that Wolbachia infection reduces total cholesterol levels in mosquitoes by 15–25 %. We then showed that cholesterol supplementation of a rat blood meal did not improve fecundity or egg viability deficits. Conversely, amino acid supplementation of sucrose before and after a sheep blood meal led to statistically significant increases in fecundity of approximately 15–20 eggs per female and egg viability of 30–40 %. This mosquito system provides the first empirical evidence of competition between Wolbachia and a host over amino acids and may suggest a general feature of Wolbachia–insect associations. These competitive processes could affect many aspects of host physiology and potentially mosquito fitness, a key concern for Wolbachia-based mosquito biocontrol.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett 281:215–220

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE 7:e38544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. O’Neill SL, Hoffmann AA, Werren JH (1997) Influential passengers. Inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford

    Google Scholar 

  4. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702–702

    Article  CAS  PubMed  Google Scholar 

  5. Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6:2753–2763

    Article  CAS  Google Scholar 

  6. Glaser RL, Meola MA (2010) The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. Plos One. doi:10.1371/journal.pone.0011977

    Google Scholar 

  7. Mousson L, Zouache K, Arias-Goeta C, Raquin V, Mavingui P et al (2012) The native Wolbachia symbionts limit transmission of dengue virus in Aedes albopictus. PLoS Negl Trop Dis 6:e1989

    Article  PubMed Central  PubMed  Google Scholar 

  8. McMeniman CJ, Lane RV, Cass BN, Fong AWC, Sidhu M et al (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323:141–144

    Article  CAS  PubMed  Google Scholar 

  9. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD et al (2011) A non-virulent Wolbachia infection blocks dengue transmission and rapidly invades Aedes aegypti populations. Nature 476:450–455

    Article  CAS  PubMed  Google Scholar 

  10. Xi Z, Khoo CC, Dobson SL (2005) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310:326–328

    Article  CAS  PubMed  Google Scholar 

  11. Bian G, Zhou G, Lu P, Xi Z (2013) Replacing a native Wolbachia with a novel strain results in an increase in endosymbiont load and resistance to dengue virus in a mosquito vector. PLoS Negl Trop Dis 7:e22250

    Article  Google Scholar 

  12. McGraw EA, O’Neill SL (2013) Beyond insecticides: new thinking on an ancient problem. Nat Rev Microbiol 11:181–193

    Article  CAS  PubMed  Google Scholar 

  13. Bian GW, Xu Y, Lu P, Xie Y, Xi ZY (2010) The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog 6:e1000833

    Article  PubMed Central  PubMed  Google Scholar 

  14. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu GJ, Pyke AT et al (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139:1268–1278

    Article  PubMed  Google Scholar 

  15. Kambris Z, Cook PE, Phuc HK, Sinkins SP (2009) Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326:134–136

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. van den Hurk AF, Hall-Mendelin S, Pyke AT, Frentiu FD, McElroy K et al (2012) Impact of Wolbachia on infection with Chikungunya and Yellow Fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis 6:e1892

    Article  PubMed Central  PubMed  Google Scholar 

  17. Osborne S, Iturbe-Ormaetxe I, Brownlie J, O’Neill S, Johnson K (2012) Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 78:6922–6929

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Rancès E, Ye YH, Woolfit M, McGraw EA, O’Neill SL (2012) The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 8:e1002548

    Article  PubMed Central  PubMed  Google Scholar 

  19. Ye Y, Woolfit M, Rances E, O’Neill S, McGraw E (2013) Wolbachia-associated bacterial protection in the mosquito Aedes aegypti. PLoS Negl Trop Dis 7:e2362

  20. Champion de Crespigny F, Wedell N (2006) Wolbachia infection reduces sperm competitive ability in an insect. Proc Biol Sci 273:1455–1458

    Article  PubMed Central  PubMed  Google Scholar 

  21. Almeida F, Moura A, Cardoso A, Winter C, Bijovsky A et al (2011) Effects of Wolbachia on fitness of Culex quinquefasciatus (Diptera: Culicidae). Infect Genet Evol 11:2138–2143

    Article  PubMed  Google Scholar 

  22. Gavotte L, Mercer D, Stoeckle J, Dobson S (2011) Costs and benefits of Wolbachia infection in immature Aedes albopictus depend upon sex and competition level. J Invertebr Pathol 105:341–346

    Article  Google Scholar 

  23. Fry A, Rand D (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56:1976–1981

    Article  PubMed  Google Scholar 

  24. Min KT, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci U S A 94:10792–10796

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. McMeniman CJ, O’Neill SL (2010) A virulent Wolbachia infection decreases the viability of the dengue vector Aedes aegypti during periods of embryonic quiescence. PLoS Negl Trop Dis 4:e748

    Article  PubMed Central  PubMed  Google Scholar 

  26. Turley AP, Moreira LA, O’Neill SL, McGraw EA (2009) Wolbachia infection reduces blood-feeding success in the dengue fever mosquito, Aedes aegypti. PLoS Negl Trop Dis 3:e516

    Article  PubMed Central  PubMed  Google Scholar 

  27. Foster J, Ganatra M, Kamal I, Ware J, Makarova K et al (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3:e121

    Article  PubMed Central  PubMed  Google Scholar 

  28. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R et al (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2:327–341

    Article  CAS  Google Scholar 

  29. Spielman A, Gwadz RW, Anderson WA (1971) Ecdysone-initiated ovarian development in mosquitoes. J Insect Physiol 17:1807–1814

    Article  CAS  PubMed  Google Scholar 

  30. Uchida K, Ohmori D, Eshita Y, Oda T, Kato Y et al (1998) Ovarian development induced in decapitated female Culex pipiens pallens mosquitoes by infusion of physiological quantities of 20-hydroxyecdysone together with amino acids. J Insect Physiol 44:525–528

    Article  CAS  PubMed  Google Scholar 

  31. Ziegler R, Ibrahim MM (2001) Formation of lipid reserves in fat body and eggs of the yellow fever mosquito, Aedes aegypti. J Insect Physiol 47:623–627

    Article  CAS  PubMed  Google Scholar 

  32. McMeniman CJ, Hughes GL, O’Neill SL (2011) A Wolbachia symbiont in Aedes aegypti disrupts mosquito egg development to a greater extent when mosquitoes feed on nonhuman versus human blood. J Med Entomol 48:76–84

    Article  PubMed  Google Scholar 

  33. Chang YYH, Judson CL (1979) Amino acid composition of human and guinea pig blood proteins, and ovarian proteins of the Yellow Fever mosquito Aedes aegypti and their effects on the mosquito egg production. Comp Biochem Physiol A 62:753–755

    Article  Google Scholar 

  34. Chapman MJ (1980) Animal lipoproteins—chemistry, structure, and comparative aspects. J Lipid Res 21:789–853

    CAS  PubMed  Google Scholar 

  35. Gerber FJ, Barnard DR, Ward RA (1994) Manual for mosquito rearing and experimental techniques. Am Mosq Control Assoc Bull 5:1–98

    Google Scholar 

  36. Fluegel ML, Parker TJ, Pallanck LJ (2006) Mutations of a Drosophila NPC1 gene confer sterol and ecdysone metabolic defects. Genetics 172:185–196

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Uchida K, Oda T, Matsuoka H, Moribayashi A, Ohmori D et al (2001) Induction of oogenesis in mosquitoes (Diptera: Culicidae) by infusion of the hemocoel with amino acids. J Med Entomol 38:572–575

    Article  CAS  PubMed  Google Scholar 

  38. Attardo GM, Hansen IA, Shiao SH, Raikhel AS (2006) Identification of two cationic amino acid transporters required for nutritional signaling during mosquito reproduction. J Exp Biol 209:3071–3078

    Article  CAS  PubMed  Google Scholar 

  39. Hagedorn HH, Fallon AM, Laufer H (1973) Vitellogenin synthesis by the fat body of the mosquito Aedes aegypti: evidence of transcriptional control. Dev Biol 31:285–294

    Article  CAS  PubMed  Google Scholar 

  40. Simon P (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19:1439–1440

    Article  CAS  PubMed  Google Scholar 

  41. Cook PE, Hugo LE, Iturbe-Ormaetxe I, Williams CR, Chenoweth SF et al (2006) The use of transcriptional profiles to predict adult mosquito age under field conditions. Proc Natl Acad Sci U S A 103:18060–18065

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Hansen IA, Attardo GM, Park JH, Peng Q, Raikhel AS (2004) Target of rapamycin-mediated amino acid signaling in mosquito anautogeny. Proc Natl Acad Sci U S A 101:10626–10631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Lin MQ, Rikihisa Y (2003) Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid a biosynthesis and incorporate cholesterol for their survival. Infect Immun 71:5324–5331

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Watarai M, Makino S, Michikawa M, Yanagisawa K, Murakami S et al (2002) Macrophage plasma membrane cholesterol contributes to Brucella abortus infection of mice. Infect Immun 70:4818–4825

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Xiong QM, Lin MQ, Rikihisa Y (2009) Cholesterol-dependent Anaplasma phagocytophilum exploits the low-density lipoprotein uptake pathway. PLoS Pathog 5:e1000329

    Article  PubMed Central  PubMed  Google Scholar 

  46. Cho K-O, Kim G-W, Lee O-K (2011) Wolbachia bacteria reside in host golgi-related vesicles whose position is regulated by polarity proteins. PLoS ONE 6:e22703

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Carabeo RA, Mead DJ, Hackstadt T (2003) Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci U S A 100:6771–6776

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Howe D, Heinzen RA (2006) Coxiella burnetii inhabits a cholesterol-rich vacuole and influences cellular cholesterol metabolism. Cell Microbiol 8:496–507

    Article  CAS  PubMed  Google Scholar 

  49. Pralle A, Keller P, Florin EL, Simons K, Horber JKH (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148:997–1007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Gasque G, Labarca P, Darszon A (2005) Cholesterol-depleting compounds modulate K+-currents in Drosophila kenyon cells. FEBS Lett 579:5129–5134

    Article  CAS  PubMed  Google Scholar 

  51. Foster JD, Adkins SD, Lever JR, Vaughan RA (2008) Phorbol ester induced trafficking-independent regulation and enhanced phosphorylation of the dopamine transporter associated with membrane rafts and cholesterol. J Neurochem 105:1683–1699

    Article  CAS  PubMed  Google Scholar 

  52. Moreira LA, Saig E, Turley AP, Ribeiro JMC, O’Neill SL et al (2009) Human probing behavior of Aedes aegypti when infected with a life-shortening strain of Wolbachia. PLoS Negl Trop Dis 3:e568

    Article  PubMed Central  PubMed  Google Scholar 

  53. Briegel H (1990) Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J Insect Physiol 36:165–172

    Article  Google Scholar 

  54. Breitling R (2007) Greased hedgehogs: new links between hedgehog signaling and cholesterol metabolism. Bioessays 29:1085–1094

    Article  CAS  PubMed  Google Scholar 

  55. Evans O, Caragata EP, McMeniman CJ, Woolfit M, Green DC et al (2009) Increased locomotor activity and metabolism of Aedes aegypti infected with a life-shortening strain of Wolbachia pipientis. J Exp Biol 212:1436–1441

    Article  PubMed Central  PubMed  Google Scholar 

  56. Ziegler R, Van Antwerpen R (2006) Lipid uptake by insect oocytes. Insect Biochem Mol Biol 36:264–272

    Article  CAS  PubMed  Google Scholar 

  57. Caragata EP, Rances E, Hedges LM, Gofton AW, Johnson KN et al (2013) Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog 9:e1003459

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Stallings DM, Hepburn DD, Hannah M, Vincent JB, O’Donnell J (2006) Nutritional supplement chromium picolinate generates chromosomal aberrations and impedes progeny development in Drosophila melanogaster. Mutat Res 610:101–113

    Article  CAS  PubMed  Google Scholar 

  59. Douglas AE (1998) Nutritional interactions in insect–microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    Article  CAS  PubMed  Google Scholar 

  60. Briegel H (1986) Protein catabolism and nitrogen partitioning during oogenesis in the mosquito Aedes aegypti. J Insect Physiol 32:455–462

    Article  Google Scholar 

  61. Zhou G, Flowers M, Friedrich K, Horton J, Pennington J et al (2004) Metabolic fate of [14C]-labeled meal protein amino acids in Aedes aegypti mosquitoes. J Insect Physiol 50:337–349

    Article  CAS  PubMed  Google Scholar 

  62. Mostowy WM, Foster WA (2004) Antagonistic effects of energy status on meal size and egg-batch size of Aedes aegypti (Diptera: Culicidae). J Vector Ecol 29:84–93

    PubMed  Google Scholar 

  63. Shiao SH, Hansen IA, Zhu J, Sieglaff DH, Raikhel AS (2008) Juvenile hormone connects larval nutrition with target of rapamycin signaling in the mosquito Aedes aegypti. J Insect Physiol 54:231–239

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Zhou G, Pennington JE, Wells MA (2004) Utilization of pre-existing energy stores of female Aedes aegypti mosquitoes during the first gonotrophic cycle. Insect Biochem Mol Biol 34:919–925

    Article  CAS  PubMed  Google Scholar 

  65. Ponnusamy L, Xu N, Nojima S, Wesson DM, Schal C et al (2008) Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proc Natl Acad Sci U S A 105:9262–9267

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  66. Canyon DV, Hii JL, Muller R (1999) Adaptation of Aedes aegypti (Diptera: Culicidae) oviposition behavior in response to humidity and diet. J Insect Physiol 45:959–964

    Article  CAS  PubMed  Google Scholar 

  67. Bandi C, McCall JW, Genchi C, Corona S, Venco L et al (1999) Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 29:357–364

    Article  CAS  PubMed  Google Scholar 

  68. Dobson SL, Rattanadechakul W, Marsland EJ (2004) Fitness advantage and cytoplasmic incompatibility in Wolbachia single- and superinfected Aedes albopictus. Heredity 93:135–142

    Article  CAS  PubMed  Google Scholar 

  69. Grenier S, Gomes SM, Pintureau B, Lassabliere F, Bolland P (2002) Use of tetracycline in larval diet to study the effect of Wolbachia on host fecundity and clarify taxonomic status of Trichogramma species in cured bisexual lines. J Invertebr Pathol 80:13–21

    Article  PubMed  Google Scholar 

  70. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5:997–1005

    Article  CAS  Google Scholar 

  71. Fleury F, Vavre F, Ris N, Fouillet P, Bouletreau M (2000) Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. Parasitology 121:493–500

    Article  PubMed  Google Scholar 

  72. Rigaud T, Moreau J, Juchault P (1999) Wolbachia infection in the terrestrial isopod Oniscus asellus: sex ratio distortion and effect on fecundity. Heredity 83:469–475

    Article  PubMed  Google Scholar 

  73. Sarakatsanou A, Diamantidis AD, Papanastasiou SA, Bourtzis K, Papadopoulos NT (2011) Effects of Wolbachia on fitness of the Mediterranean fruit fly (Diptera: Tephritidae). J Appl Entomol 135:554–563

    Article  Google Scholar 

  74. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH et al (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454–U107

    Article  CAS  PubMed  Google Scholar 

  75. Rancès E, Johnson TK, Popovici J, Iturbe-Ormaetxe I, Zakir T et al (2013) The Toll and Imd pathways are not required for Wolbachia mediated dengue virus interference. J Virol. doi:10.1128/JVI.01522-13

    PubMed Central  PubMed  Google Scholar 

  76. Lee CJ, Lin HR, Liao CL, Lin YL (2008) Cholesterol effectively blocks entry of flavivirus. J Virol 82:6470–6480

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  77. Sasao F, Igarashi A, Fukai K (1980) Amino acid requirements for the growth of Aedes albopictus clone C6-36 cells and for the production of Dengue and Chikungunya viruses in the infected Cells. Microbiol Immunol 24:915–924

    Article  CAS  PubMed  Google Scholar 

  78. Vollmer J, Schiefer A, Schneider T, Julicher K, Johnston KL et al (2013) Requirement of lipid II biosynthesis for cell division in cell wall-less Wolbachia, endobacteria of arthropods and filarial nematodes. Int J Med Microb. doi:10.1016/j.ijmm.2013.01.002

    Google Scholar 

  79. Heaton NS, Perera R, Berger KL, Khadka S, LaCount DJ et al (2010) Dengue virus nonstructural protein 3 redistributes fatty acid synthase to sites of viral replication and increases cellular fatty acid synthesis. Proc Natl Acad Sci U S A 107:17345–17350

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  80. Perera R, Riley C, Isaac G, Hopf-Jannasch AS, Moore RJ et al (2012) Dengue virus infection perturbs lipid homeostasis in infected mosquito cells. PLoS Pathog 8:e1002584

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  81. Alabaster A, Isoe J, Zhou G, Lee A, Murphy A et al (2011) Deficiencies in acetyl-CoA carboxylase and fatty acid synthase 1 differentially affect eggshell formation and blood meal digestion in Aedes aegypti. Insect Biochem Mol Biol 41:946–955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  82. Darby AC, Armstrong SD, Bah GS, Kaur G, Hughes MA et al (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res 22:2467–2477

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  83. McGarry HF, Egerton GL, Taylor MJ (2004) Population dynamics of Wolbachia bacterial endosymbionts in Brugia malayi. Mol Biochem Parasitol 135:57–67

    Article  CAS  PubMed  Google Scholar 

  84. Dunning Hotopp JC, Lin M, Madupu R, Crabtree J, Angiuoli SV et al (2006) Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2:e21

    Article  PubMed Central  PubMed  Google Scholar 

  85. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86

    Article  CAS  PubMed  Google Scholar 

  86. Zientz E, Dandekar T, Gross R (2004) Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol Mol Biol Rev 68:745–770

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments and Funding

The authors would like to thank Nichola Kenny, Jenny Gough, Yin San Leong, Eliane Moreira and Jack Godrich for technical assistance, Kym French and Sue Rabocyzj for caring for bleeding rats, and the UQ Health Service for bleeding human volunteers. This work was conducted in accordance with The University of Queensland human ethics project number 2007001379 and animal ethics project number SBS/452/09/NIH. This work was supported by grants from the Foundation for the National Institute of Health through the Grand Challenges in Global Health Initiative of the Bill and Melinda Gates Foundation and the National Health and Medical Research Council of Australia.

Author information

Author notes

  1. Edwige Rancès

    Present address: Unité d’entomologie Médicale, Institut Pasteur de Guyane, Cayenne, Guyane française, France

Authors and Affiliations

  1. School of Biological Sciences, Monash University, Melbourne, VIC, Australia, 3800

    Eric P. Caragata, Edwige Rancès, Scott L. O’Neill & Elizabeth A. McGraw

  2. School of Biological Sciences, The University of Queensland, Brisbane, QLD, Australia, 4072

    Eric P. Caragata

Authors
  1. Eric P. Caragata
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edwige Rancès
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Scott L. O’Neill
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizabeth A. McGraw
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elizabeth A. McGraw.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caragata, E.P., Rancès, E., O’Neill, S.L. et al. Competition for Amino Acids Between Wolbachia and the Mosquito Host, Aedes aegypti . Microb Ecol 67, 205–218 (2014). https://doi.org/10.1007/s00248-013-0339-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0339-4

Keywords

Search

Navigation