Larval exposure to Francisella tularensis LVS affects fitness of the mosquito Culex quinquefasciatus

FEMS Microbiology Ecology

Volumn 78, Issue 3, 2011, Pages 520-530

  Mahajan, Uma V ^a   Gravgaard, Jonathan ^a   Turnbull, Matthew ^a   Jacobs, David B ^a   McNealy, Tamara L ^a  

^a CLEMSON UNIVERSITY   (United States)

Author keywords

Biofilm; Francisella tularensis; Mosquito larvae

Indexed keywords

ADULT; AQUATIC ORGANISM; BACTERIAL DISEASE; BACTERIUM; BIOFILM; BIOLOGICAL INVASION; FECUNDITY; FITNESS; HOST-PATHOGEN INTERACTION; LARVA; MOSQUITO; PROTOZOAN; PUPATION; SURVIVAL;

ANIMAL; ARTICLE; BIOFILM; CULEX; FEMALE; FERTILITY; FRANCISELLA TULARENSIS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; LARVA; MALE; MICROBIOLOGY; PATHOGENICITY; TULAREMIA;

ANIMALS; BIOFILMS; CULEX; FEMALE; FERTILITY; FRANCISELLA TULARENSIS; HOST-PATHOGEN INTERACTIONS; LARVA; MALE; TULAREMIA; WATER MICROBIOLOGY;

AVES; BACTERIA (MICROORGANISMS); CULEX PIPIENS QUINQUEFASCIATUS; FRANCISELLA TULARENSIS; HEXAPODA; INVERTEBRATA; MAMMALIA; PROTOZOA; REPTILIA;

EID: 81155144724     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2011.01182.x     Document Type: Article

References (48)

1. Abd H, Johansson T, Golovliov I, Sandstrom G & Forsman M (2003) Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl Environ Microb 69: 600-606.
2. Alam M, Sultana M, Nair GB, Sack RB, Sack DA, Siddique AK, Ali A, Huq A & Colwell RR (2006) Toxigenic Vibrio cholerae in the aquatic environment of Mathbaria, Bangladesh. Appl Environ Microb 72: 2849-2855.
3. Amer L, Bishop B & Hoek M (2010) Antimicrobial and antibiofilm activity of cathelicidins and short, synthetic peptides against Francisella. Biochem Biophys Res Commun 396: 246-291.
4. Aperis G, Fuchs BB, Anderson CA, Warner JE, Calderwood SB & Mylonakis E (2007) Galleria mellonella as a model host to study infection by the Francisella tularensis live vaccine strain. Microb Infect 9: 729-734.
5. Barker J & Brown MR (1994) Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology 140: 1253-1259.
6. Bradley TJ & Nayar JK (1985) Intracellular melanization of the larvae of Dirofilaria immitis in the malpighian tubules of the mosquito Aedes sollicitans. J Invertebr Pathol 45: 339-345.
7. Christenson B (1984) An outbreak of tularemia in the northern part of central Sweden. Scand J Infect Dis 16: 285-290.
8. Cirillo JD, Cirillo SL, Yan L, Bermudez LE, Falkow S & Tompkins LS (1999) Intracellular growth in Acanthamoeba castellanii affects monocyte entry mechanisms and enhances virulence of Legionella pneumophila. Infect Immun 67: 4427-4434.
9. Declerck P (2010) Biofilms: the environmental playground of Legionella pneumophila. Environ Microbiol 12: 557-566.
10. Duodu S & Colquhoun D (2010) Monitoring the survival of fish-pathogenic Francisella in water microcosms. FEMS Microbiol Ecol 74: 534-541.
11. Durham-Colleran MW, Verhoeven AB & Van Hoek ML (2010) Francisella novicida forms in vitro biofilms mediated by an orphan response regulator. Microbial Ecol 59: 457-465.
12. Eliasson H & Back E (2007) Tularemia in an emergent area in Sweden: an analysis of 234 cases in five years. Scand J Infect Dis 39: 880-889.
13. Eliasson H, Lindback J, Nuorti JP, Arneborn M, Giesecke J & Tegnell A (2002) The 2000 tularemia outbreak: a case-control study of risk factors in disease-endemic and emergent areas, Sweden. Emerg Infect Dis 8: 956-960.
14. EPA US (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. Report #: EPA-821-R-02-012. 5: 41.
15. Freitak D, Wheat CW, Heckel DG & Vogel H (2007) Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni. BMC Biol 5: 1-13.
16. Gravgaard JC, Turnbull MW & McNealy TL (2010) A novel technique for feeding and confirming uptake of bacteria in larvae of the southern house mosquito Culex quinquefasciatus (Diptera: Culicidae). Fla Entomol 93: 577-583.
17. Gurycova D (1998) First isolation of Francisella tularensis subsp tularensis in Europe. Eur J Epidemiol 14: 797-802.
18. Hahn MW & Höfle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35: 113-121.
19. Hall-Stoodley L, Costerton JW & Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nature Rev Microbiol 2: 95-108.
20. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK & Molin S (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395-2407.
21. Huws SA, McBain AJ & Gilbert P (2005) Protozoan grazing and its impact upon population dynamics in biofilm communities. J Appl Microbiol 98: 238-244.
22. Islam MS & Dobson SL (2006) Wolbachia effects on Aedes albopictus (Diptera: Culicidae) immature survivorship and development. J Med Entomol 43: 689-695.
23. Kartman L (1953) Factors influencing infection of the mosquito with Dirofilaria immitis (Leidy, 1856). Exp Parasit 2: 27-78.
24. Kaufman MG, Walker ED, Smith TW, Merritt RW & Klug MJ (1999) Effects of larval mosquitoes (Aedes triseriatus) and stemflow on microbial community dynamics in container habitats. Appl Environ Microb 65: 2661-2673.
25. Kaufman MG, Bland SN, Worthen ME, Walker ED & Klug MJ (2001) Bacterial and fungal biomass responses to feeding by larval Aedes triseratus (Diptera: Culicidae). J Med Entomol 38: 711-719.
26. Kaufman MG, Goodfriend W, Kohler-Garrigan A, Walker ED & Klug MJ (2002) Soluble nutrient effects on microbial communities and mosquito production in Ochlerotatus triseriatus habitats. Aquat Microb Ecol 29: 73-88.
27. Keim P, Johansson A & Wagner DM (2007) Molecular epidemiology evolution and ecology of Francisella. Ann NY Acad Sci 1105: 30-66.
28. Lundström JO, Andersson AC, Backman S, Schafer ML, Forsman M & Thelaus J (2011) Transstadial transmission of Francisella tularensis holarctica in mosquitoes, Sweden. Emerg Infect Dis 17: 794-799.
29. Mandal SK, Ghosh A, Bhattacharjee I & Chandra G (2008) Biocontrol efficiency of odonate nymphs against larvae of the mosquito Culex quinquefasciatus Say 1823. Acta Trop 106: 109-114.
30. McGettigan J, McLennan RK, Broderick KE et al. (2005) Insect renal tubules constitute a cell-autonomous immune system that protects the organism against bacterial infection. Insect Biochem Molec 35: 741-754.
31. Melillo A, Sledjeski DD, Lipski S, Wooten RM, Basrur V & Lafontaine ER (2006) Identification of a Francisella tularensis LVS outer membrane protein that confers adherence to A549 human lung cells. FEMS Microbiol Lett 263: 102-108.
32. Merritt RW, Dadd RH & Walker ED (1992) Feeding behavior natural food and nutritional relationships of larval mosquitoes. Annu Rev Entomol 37: 349-376.
33. Miller LA, Beebe JL, Butler JC, Martin W, Benson R, Hoffman RE & Fields BS (1993) Use of polymerase chain reaction in an epidemiologic investigation of Pontiac fever. J Infect Dis 168: 769-772.
34. Nnakumusana ES (1985) Laboratory infection of mosquito larvae by entomopathogenic fungi with particular reference to Aspergillus parasiticus and its effects on fecundity and longevity of mosquitoes exposed to spore infections in larval stages. Curr Sci India 54: 1221-1228.
35. Peck GW & Walton WE (2006) Effect of bacterial quality and density on growth and whole body stoichiometry of Culex quinquefasciatus and Culex tarsalis (Diptera: Culicidae). J Med Entomol 43: 25-33.
36. Philip CB & Parker RR (1932) Public health weekly reports for October 21 1932. Public Health Rep 47: 2077-2103.
37. Prasad H, Prasad RN & Haq S (1993) Control of mosquito breeding through Gambusia affinis in rice fields. Indian J Malariol 30: 57-65.
38. Read A, Vogl SJ, Hueffer K, Gallagher LA & Happ GM (2008) Francisella genes required for replication in mosquito cells. J Med Entomol 45: 1108-1116.
39. Rickard AH, Gilbert P, High NJ, Kolenbrander PE & Handley PS (2003) Bacterial co-aggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 11: 94-100.
40. Roth O & Kurtz J (2008) The stimulation of immune defense accelerates development in the red flour beetle (Tribolium castaneum). J Evolution Biol 21: 1703-1710.
41. Santic M, Akimana C, Asare R, Kouokam JC, Atay S & Kwaik YA (2009) Intracellular fate of Francisella tularensis within arthropod-derived cells. Environ Microbiol 11: 1473-1481.
42. Sinclair R, Boone SA, Greenberg D, Keim P & Gerba CP (2008) Persistence of category A select agents in the environment. Appl Environ Microb 74: 555-563.
43. Triebenbach AN, Vogl SJ, Lotspeich-Cole L, Sikes DS, Happ GM & Hueffer K (2010) Detection of Francisella tularensis in Alaskan mosquitoes (Diptera: Culicidae) and assessment of a laboratory model for transmission. J Med Entomol 47: 639-648.
44. Vezzulli L, Pruzzo C, Huq A & Colwell RR (2010) Environmental reservoirs of Vibrio cholerae and their role in cholera. Environ Microbiol Reports 2: 27-33.
45. Vonkavaara M, Telepnev MV, Ryden P, Sjostedt A & Stoven S (2008) Drosophila melanogaster as a model for elucidating the pathogenicity of Francisella tularensis. Cell Microbiol 10: 1327-1338.
46. Wallace JR, Gordon MC, Hartsell L, Mosi L, Benbow ME, Merritt RW & Small PL (2010) Interaction of Mycobacterium ulcerans with mosquito species: implications for transmission and trophic relationships. Appl Environ Microb 76: 6215-6222.
47. Yen CH (1938) Studies on Dirofilaria immitis Leidy, with special reference to the susceptibility of some Minnesota species of mosquitoes to the infection. J Parasit 24: 189-205.
48. Yen JH & Barr RA (1973) The etiological agent of cytoplasmic incompatibility in Culex pipiens. J Invertebr Pathol 22: 242-250.