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

Microbial Ecology

Volumn 67, Issue 1, 2014, Pages 205-218

  Caragata, Eric P ^a,b   Rancès, Edwige ^a,b,c   O'Neill, Scott L ^a,b   McGraw, Elizabeth A ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c INSTITUT PASTEUR DE LA GUYANE   (French Guiana)

Author keywords

[No Author keywords available]

Indexed keywords

AEDES AEGYPTI; HEXAPODA; OVIS ARIES; RATTUS; WOLBACHIA;

AMINO ACID; CHOLESTEROL;

AEDES; ANIMAL; ARTICLE; FEMALE; FERTILITY; HUMAN; LEWIS RAT; METABOLISM; MICROBIOLOGY; OOCYTE; PHYSIOLOGY; RAT; SHEEP; SYMBIOSIS; WOLBACHIA;

AEDES; AMINO ACIDS; ANIMALS; CHOLESTEROL; FEMALE; FERTILITY; HUMANS; OVUM; RATS; RATS, INBRED LEW; SHEEP; SYMBIOSIS; WOLBACHIA;

EID: 84893777291     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-013-0339-4     Document Type: Article

References (86)

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.
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.
3. O'Neill SL, Hoffmann AA, Werren JH (1997) Influential passengers. Inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford.
4. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322: 702-702.
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.
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.
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.
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.
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.
10. Xi Z, Khoo CC, Dobson SL (2005) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310: 326-328.
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.
12. McGraw EA, O'Neill SL (2013) Beyond insecticides: new thinking on an ancient problem. Nat Rev Microbiol 11: 181-193.
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.
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.
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.
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.
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.
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.
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.
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.
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.
23. Fry A, Rand D (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56: 1976-1981.
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.
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.
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.
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.
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.
29. Spielman A, Gwadz RW, Anderson WA (1971) Ecdysone-initiated ovarian development in mosquitoes. J Insect Physiol 17: 1807-1814.
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.
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.
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.
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.
34. Chapman MJ (1980) Animal lipoproteins-chemistry, structure, and comparative aspects. J Lipid Res 21: 789-853.
35. Gerber FJ, Barnard DR, Ward RA (1994) Manual for mosquito rearing and experimental techniques. Am Mosq Control Assoc Bull 5: 1-98.
36. Fluegel ML, Parker TJ, Pallanck LJ (2006) Mutations of a Drosophila NPC1 gene confer sterol and ecdysone metabolic defects. Genetics 172: 185-196.
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.
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.
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.
40. Simon P (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19: 1439-1440.
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.
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.
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.
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.
45. Xiong QM, Lin MQ, Rikihisa Y (2009) Cholesterol-dependent Anaplasma phagocytophilum exploits the low-density lipoprotein uptake pathway. PLoS Pathog 5: e1000329.
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.
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.
48. Howe D, Heinzen RA (2006) Coxiella burnetii inhabits a cholesterol-rich vacuole and influences cellular cholesterol metabolism. Cell Microbiol 8: 496-507.
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.
50. Gasque G, Labarca P, Darszon A (2005) Cholesterol-depleting compounds modulate K+-currents in Drosophila kenyon cells. FEBS Lett 579: 5129-5134.
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.
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.
53. Briegel H (1990) Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J Insect Physiol 36: 165-172.
54. Breitling R (2007) Greased hedgehogs: new links between hedgehog signaling and cholesterol metabolism. Bioessays 29: 1085-1094.
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.
56. Ziegler R, van Antwerpen R (2006) Lipid uptake by insect oocytes. Insect Biochem Mol Biol 36: 264-272.
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.
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.
59. Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43: 17-37.
60. Briegel H (1986) Protein catabolism and nitrogen partitioning during oogenesis in the mosquito Aedes aegypti. J Insect Physiol 32: 455-462.
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.
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.
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.
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.
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.
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.
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.
68. Dobson SL, Rattanadechakul W, Marsland EJ (2004) Fitness advantage and cytoplasmic incompatibility in Wolbachia single- and superinfected Aedes albopictus. Heredity 93: 135-142.
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.
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.
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.
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.
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.
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.
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.
76. Lee CJ, Lin HR, Liao CL, Lin YL (2008) Cholesterol effectively blocks entry of flavivirus. J Virol 82: 6470-6480.
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.
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.
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.
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.
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.
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.
83. McGarry HF, Egerton GL, Taylor MJ (2004) Population dynamics of Wolbachia bacterial endosymbionts in Brugia malayi. Mol Biochem Parasitol 135: 57-67.
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.
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.
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.