Effect of quorum sensing by Staphylococcus epidermidis on the attraction response of female adult yellow fever mosquitoes, Aedes aegypti aegypti (linnaeus) (diptera: Culicidae), to a blood-feeding source

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Zhang, Xinyang ^a,b   Crippen, Tawni L ^c   Coates, Craig J ^a   Wood, Thomas K ^d   Tomberlin, Jeffery K ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLE; VOLATILE ORGANIC COMPOUND;

ADULT; AEDES AEGYPTI; AGR GENE; ANIMAL COMMUNICATION; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; FEEDING ECOLOGY; FEMALE; GENE CONTROL; GENE EXPRESSION; HOST PATHOGEN INTERACTION; NONHUMAN; QUORUM SENSING; SANGUIVORE; STAPHYLOCOCCUS EPIDERMIDIS; SYMBIOSIS; WILD TYPE; AEDES; ANIMAL; HUMAN; INSECT VECTOR; PHYSIOLOGY; TRANSMISSION; YELLOW FEVER;

AEDES; ANIMALS; HUMANS; INSECT VECTORS; QUORUM SENSING; STAPHYLOCOCCUS EPIDERMIDIS; VOLATILE ORGANIC COMPOUNDS; YELLOW FEVER;

EID: 84956876194     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143950     Document Type: Article

References (61)

1. Eldridge BF, Edman JD. Introduction to Medical Entomology. Medical Entomology: Springer; 2000. p. 1-12.
2. Becker N, Petrić D, Boase C, Lane J, Zgomba M, Dahl C, et al. Mosquitoes and their Control: Springer; 2010.
3. Eldridge BF, Edman JD. Medical Entomology: A Textbook on Public Health and Veterinary Problems Caused by Arthropods: Springer Science & Business Media; 2003.
4. Gabrieli P, Smidler A, Catteruccia F. Engineering the control of mosquito-borne infectious diseases. Genome Biology. 2014; 15(11):535. doi: 10.1186/s13059-014-0535-7 PMID: 25418061
5. Takken W, Knols BG. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annual Review of Entomology. 1999; 44(1):131-57.
6. Shelley WB, Hurley HJ, NICHOLS AC. Axillary odor: Experimental study of the role of bacteria, apocrine sweat, and deodorants. Ama archives of Dermatology and Syphilology. 1953; 68(4):430-46.
7. Verhulst NO, Takken W, Dicke M, Schraa G, Smallegange RC. Chemical ecology of interactions between human skin microbiota and mosquitoes. FEMS Microbiology Ecology. 2010; 74(1):1-9. doi: 10.1111/j.1574-6941.2010.00908.x PMID: 20840217
8. De Jong R, Knols B. Selection of biting sites on man by two malaria mosquito species. Experientia. 1995; 51(1):80-4. PMID: 7843335
9. Takken W. The role of olfaction in host-seeking of mosquitoes: A review. International Journal of Tropical Insect Science. 1991; 12(1-2-3):287-95.
10. Bernier UR, Kline DL, Barnard DR, Schreck CE, Yost RA. Analysis of human skin emanations by gas chromatography/mass spectrometry. 2. Identification of volatile compounds that are candidate attractants for the yellow fever mosquito (Aedes aegypti). Analytical Chemistry. 2000; 72(4):747-56. PMID: 10701259
11. Geier M, Bosch OJ, Boeckh J. Ammonia as an attractive component of host odour for the yellow fever mosquito, Aedes aegypti. Chemical Senses. 1999; 24(6):647-53. PMID: 10587497
12. Verhulst NO, Beijleveld H, Knols BG, Takken W, Schraa G, Bouwmeester HJ, et al. Cultured skin microbiota attracts malaria mosquitoes. Malaria Journal. 2009; 8(1):302.
13. Waters CM, Bassler BL. Quorum sensing: Cell-to-cell communication in bacteria. Annual Review of Cell and Developmental Biology. 2005; 21:319-46. PMID: 16212498
14. Sturgill G, Rather PN. Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Molecular Microbiology. 2004; 51(2):437-46. Epub 2004/02/06. PMID: 14756784
15. Lee J, Zhang X-S, Hegde M, Bentley WE, Jayaraman A, Wood TK. Indole cell signaling occurs primarily at low temperatures in Escherichia coli. International Society for Microbial Ecology Journal. 2008; 2:1007-23.
16. Qiu YT, van Loon JJA, Takken W, Meijerink J, Smid HM. Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chemical Senses. 2006; 31(9):845-63. PMID: 16963500
17. Syed Z, Leal WS. Acute olfactory response of Culex mosquitoes to a human-and bird-derived attractant. Proceedings of the National Academy of Sciences. 2009; 106(44):18803-8.
18. Carey AF, Wang G, Su C-Y, Zwiebel LJ, Carlson JR. Odorant reception in the malaria mosquito Anopheles gambiae. Nature. 2010; 464(7285):66-71. doi: 10.1038/nature08834 PMID: 20130575
19. Cork A, editor Olfactory basis of host location by mosquitoes and other haematophagous Diptera. Olfaction in mosquitoes-host interactions Ciba Foundation Symposium; 1996.
20. Qiu Y, Smallegange R, Hoppe S, Van Loon J, Bakker EJ, Takken W. Behavioural and electrophysiological responses of the malaria mosquito Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) to human skin emanations. Medical and veterinary entomology. 2004; 18(4):429-38. PMID: 15642010
21. Schleifer KH, Kloos WE. Isolation and characterization of Staphylococci from human skin I. Amended descriptions of Staphylococcus epidermidis and Staphylococcus saprophyticus and descriptions of three new species: Staphylococcus cohnii, Staphylococcus haemolyticus, and Staphylococcus xylosus. International Journal of Systematic Bacteriology. 1975; 25(1):50-61.
22. James A, Hyliands D, Johnston H. Generation of volatile fatty acids by axillary bacteria1. International Journal of Cosmetic Science. 2004; 26(3):149-56. doi: 10.1111/j.1467-2494.2004.00214.x PMID: 18494871
23. Kong K-F, Vuong C, Otto M. Staphylococcus quorum sensing in biofilm formation and infection. International Journal of Medical Microbiology. 2006; 296(2):133-9.
24. Lowery CA, Dickerson TJ, Janda KD. Interspecies and interkingdom communication mediated by bacterial quorum sensing. Chemical Society Reviews. 2008; 37(7):1337-46. doi: 10.1039/b702781h PMID: 18568160
25. Joint I, Tait K, Callow ME, Callow JA, Milton D, Williams P, et al. Cell-to-cell communication across the prokaryote-eukaryote boundary. Science. 2002; 298(5596):1207. PMID: 12424372
26. Wu L, Estrada O, Zaborina O, Bains M, Shen L, Kohler JE, et al. Recognition of host immune activation by Pseudomonas aeruginosa. Science. 2005; 309(5735):774-7. PMID: 16051797
27. Ma Q, Fonseca A, Liu W, Fields AT, Pimsler ML, Spindola AF, et al. Proteus mirabilis interkingdom swarming signals attract blow flies. International Society for Microbial Ecology Journal. 2012; 6 (7):1356-66.
28. Chaudhury M, Skoda SR, Sagel A, Welch J. Volatiles emitted from eight wound-isolated bacteria differentially attract gravid screwworms (Diptera: Calliphoridae) to oviposit. Journal of Medical Entomology. 2010; 47(3):349-54. PMID: 20496582
29. Chaudhury M, Welch J, Alvarez LA. Responses of fertile and sterile screwworm (Diptera: Calliphoridae) flies to bovine blood inoculated with bacteria originating from screwworm-infested animal wounds. Journal of Medical Entomology. 2002; 39(1):130-4. PMID: 11931246
30. Morris MC. Tests on a new bait for flies (Diptera: Calliphoridae) causing cutaneous myiasis (flystrike) in sheep. New Zealand Journal of Agricultural Research. 2005; 48(1):151-6.
31. Vuong C, Götz F, Otto M. Construction and characterization of anagr deletion mutant of Staphylococcus epidermidis. Infection and Immunity. 2000; 68(3):1048-53. PMID: 10678906
32. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, Gordon JI. The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature. 2007; 449(7164):804. PMID: 17943116
33. Microbiology ASF. Humans have ten times more bacteria than human cells: How do microbial communities affect human health? 2008.
34. Hughes DT, Sperandio V. Inter-kingdom signalling: communication between bacteria and their hosts. Nature Reviews Microbiology. 2008; 6(2):111-20. doi: 10.1038/nrmicro1836 PMID: 18197168
35. Wang Y, Dufour YS, Carlson HK, Donohue TJ, Marletta MA, Ruby EG. H-NOX-mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri. Proceedings of the National Academy of Sciences. 2010; 107(18):8375-80.
36. Moreira CG, Sperandio V. Interplay between the QseC and QseE bacterial adrenergic sensor kinases in Salmonella enterica serovar Typhimurium pathogenesis. Infection and Immunity. 2012; 80 (12):4344-53. doi: 10.1128/IAI.00803-12 PMID: 23027532
37. Shin SC, Kim S-H, You H, Kim B, Kim AC, Lee K-A, et al. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science. 2011; 334(6056):670-4. doi: 10. 1126/science.1212782 PMID: 22053049
38. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, et al. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. The EMBO Journal. 2003; 22(15):3803-15. PMID: 12881415
39. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nature Reviews Microbiology. 2012; 10(11):735-42. doi: 10.1038/nrmicro2876 PMID: 23000955
40. Heijtz RD, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, et al. Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences. 2011; 108 (7):3047-52.
41. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proceedings of the National Academy of Sciences. 2011; 108(Supplement 1):4615-22.
42. Mayer EA. Gut feelings: The emerging biology of gut-brain communication. Nature Reviews Neuroscience. 2011; 12(8):453-66. doi: 10.1038/nrn3071 PMID: 21750565
43. Gillies M. The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): A review. Bulletin of Entomological Research. 1980; 70(04):525-32.
44. Verhulst NO, Andriessen R, Groenhagen U, Bukovinszkiné Kiss G, Schulz S, Takken W, et al. Differential attraction of malaria mosquitoes to volatile blends produced by human skin bacteria. PLoS One. 2010; 5(12):e15829. doi: 10.1371/journal.pone.0015829 PMID: 21209854
45. Smallegange RC, Verhulst NO, Takken W. Sweaty skin: An invitation to bite? Trends in parasitology. 2011; 27(4):143-8. doi: 10.1016/j.pt.2010.12.009 PMID: 21256083
46. Leyden JJ, McGinley KJ, Nordstrom KM, Webster GF. Skin microflora. Journal of Investigative Dermatology 1987; 88:65s-72s. PMID: 3102625
47. Fredricks DN. Microbial ecology of human skin in health and disease. Journal of Investigative Dermatology Symposium Proceedings 2001; 6:167-9.
48. Costello E, Lauber C, Hamady M, Fierer N, Gordon J, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009; 326:1694-7. doi: 10.1126/science. 1177486 PMID: 19892944
49. Kloos WE, Musslewhite MS. Distribution and persistence of Staphylococcus and Micrococcus species and other aerobic bacteria on human skin. Applied Microbiology 1975; 30:381-95. PMID: 810086
50. Price GD, Smith N, Carlson DA. The attraction of female mosquitoes (Anopheles quadrimaculatus Say) to stored human emanations in conjunction with adjusted levels of relative humidity, temperature, and carbon dioxide. Journal of Chemical Ecology. 1979; 5(3):383-95.
51. Davis EE, Sokolove PG. Temperature responses of antennal receptors of the mosquito, Aedes aegypti. Journal of comparative physiology. 1975; 96(3):223-36.
52. Klowden M, Blackmer J, Chambers G. Effects of larval nutrition on the host-seeking behavior of adult Aedes aegypti mosquitoes. Journal of the American Mosquito Control Association. 1988; 4(1):73-5. PMID: 3193101
53. Sumba LA, Guda TO, Deng AL, Hassanali A, Beier JC, Knols BG. Mediation of oviposition site selection in the African malaria mosquito Anopheles gambiae (Diptera: Culicidae) by semiochemicals of microbial origin. International Journal of Tropical Insect Science. 2004; 24(03):260-5.
54. Ponnusamy L, Xu N, Nojima S, Wesson DM, Schal C, Apperson CS. Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti. Proceedings of the National Academy of Sciences. 2008; 105(27):9262-7.
55. Clements A. Books reviewed: The Biology of Mosquitoes. Volume 1. Development, Nutrition and Reproduction. American Journal of Tropical Medicine and Hygiene. 1995; 52(6):579.
56. Dekker T, Takken W, Carde RT. Structure of host-odour plumes influences catch of Anopheles gambiae ss and Aedes aegypti in a dual-choice olfactometer. Physiological Entomology. 2001; 26(2):124-34.
57. Yasuno M, Tonn RJ. A study of biting habits of Aedes aegypti in Bangkok, Thailand. Bulletin of the World Health Organization. 1970; 43(2):319. PMID: 5312528
58. McClelland GAH. Observations on the mosquito, Aëdes (Stegomyia) aegypti (L.), in East Africa. I. - The biting cycle in an outdoor population at Entebbe, Uganda. Bulletin of Entomological Research. 1959; 50(02):227-35.
59. Syed Z, Leal WS. Mosquitoes smell and avoid the insect repellent DEET. Proceedings of the National Academy of Sciences. 2008; 105(36):13598-603.
60. De Jong R, Knols BG, editors. Selection of biting sites by mosquitoes. Olfaction in mosquitoes-host interactions Ciba Fundation Symposium; 1996.
61. Thomas DL, Taylor EJ. Study designs and tests for comparing resource use and availability. The Journal of Wildlife Management. 1990; 54(2):322-30.