Susceptibility of Caenorhabditis elegans to Burkholderia infection depends on prior diet and secreted bacterial attractants

PLoS ONE

Volumn 4, Issue 11, 2009, Pages

  Cooper, Vaughn S ^a   Carlson, Wendy A ^a   LiPuma, John J ^b  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; AVOIDANCE BEHAVIOR; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM ISOLATE; BURKHOLDERIA; BURKHOLDERIA AMBIFARIA; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA; BURKHOLDERIA DOLOSA; BURKHOLDERIA MULTIVORAN; BURKHOLDERIACEAE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ESCHERICHIA COLI; FOOD INTAKE; FOOD PREFERENCE; GENOTYPE; NONHUMAN; ANIMAL; ANIMAL FOOD; BURKHOLDERIA INFECTION; CELL FREE SYSTEM; CHEMISTRY; COCULTURE; GENE; GENETIC PREDISPOSITION; GENETICS; METABOLISM; PATHOGENICITY; PHENOTYPE; TIME; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); BURKHOLDERIA; BURKHOLDERIA AMBIFARIA; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA MULTIVORANS; CAENORHABDITIS ELEGANS; NEMATODA;

AGAR;

AGAR; ANIMAL FEED; ANIMALS; BURKHOLDERIA CEPACIA; BURKHOLDERIA INFECTIONS; CAENORHABDITIS ELEGANS; CELL-FREE SYSTEM; COCULTURE TECHNIQUES; ESCHERICHIA COLI; GENES, HELMINTH; GENETIC PREDISPOSITION TO DISEASE; PHENOTYPE; TIME FACTORS; VIRULENCE;

EID: 71049172529     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007961     Document Type: Article

References (62)

1. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392: 71-75.
2. Tan MW, Rahme LG, Sternberg JA, Tompkins RG, Ausubel FM (1999) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96: 2408-2413.
3. Tan MW, Ausubel FM (2000) Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. Curr Opin Microbiol 3: 29-34.
4. Aballay A, Ausubel FM (2002) Caenorhabditis elegans as a host for the study of host-pathogen interactions. Current Opinion in Microbiology 5: 97-101.
5. Forrester S, Milillo SR, Hoose WA, Wiedmann M, Schwab U (2007) Evaluation of the pathogenicity of Listeria spp. in Caenorhabditis elegans. Foodborne Pathog Dis 4: 67-73.
6. Pradel E, Zhang Y, Pujol N, Matsuyama T, Bargmann CI, et al. (2007) Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc Natl Acad Sci U S A 104: 2295-2300.
7. Sifri CD, Begun J, Ausubel FM, Calderwood SB (2003) Caenorhabditis elegans as a model host for Staphylococcus aureus pathogenesis. Infect Immun 71: 2208-2217.
8. Hinrich S, Jonathan JE (2007) The genetics of pathogen avoidance in Caenorhabditis elegans. Molecular Microbiology 66: 563-570.
9. Zhang Y, Lu H, Bargmann CI (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438: 179-184.
10. Beale E, Li G, Tan MW, Rumbaugh KP (2006) Caenorhabditis elegans senses bacterial autoinducers. Appl Environ Microbiol 72: 5135-5137.
11. Nicholas HR, Hodgkin J (2004) Responses to infection and possible recognition strategies in the innate immune system of Caenorhabditis elegans. Mol Immunol 41: 479-493.
12. Colbert HA, Bargmann CI (1997) Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. Learn Mem 4: 179-191.
13. Vanlaere E, Baldwin A, Gevers D, Henry D, De Brandt E, et al. (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59: 102-111.
14. Parke JL, Gurian-Sherman D (2001) Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 39: 225-258.
15. LiPuma JJ (2003) Burkholderia cepacia complex as human pathogens. Journal of Nematology 35: 212-217.
16. Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nature Reviews Microbiology 3: 144-156.
17. Isles A, Maclusky I, Corey M, Gold R, Prober C, et al. (1984) Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104: 206-210.
18. LiPuma JJ (1998) Burkholderia cepacia epidemiology and pathogenesis: implications for infection control. Curr Opin Pulm Med 4: 337-341.
19. LiPuma JJ (2003) Burkholderia and emerging pathogens in cystic fibrosis. Seminars in Respiratory and Critical Care Medicine 24: 681-692.
20. Cardona ST, Wopperer J, Eberl L, Valvano MA (2005) Diverse pathogenicity of Burkholderia cepacia complex strains in the Caenorhabditis elegans host model. FEMS Microbiol Lett 250: 97-104.
21. O'Quinn AL, Wiegand EM, Jeddeloh JA (2001) Burkholderia pseudomallei kills the nematode Caenorhabditis elegans using an endotoxin-mediated paralysis. Cell Microbiol 3: 381-393.
22. Smith MP, Laws TR, Atkins TP, Oyston PCF, de Pomerai DI, et al. (2002) A liquid-based method for the assessment of bacterial pathogenicity using the nematode Caenorhabditis elegans. Fems Microbiology Letters 210: 181-185.
23. Wopperer J, Cardona ST, Huber B, Jacobi CA, Valvano MA, et al. (2006) A quorum-quenching approach to investigate the conservation of quorum-sensing-regulated functions within the Burkholderia cepacia complex. Appl Environ Microbiol 72: 1579-1587.
24. Kothe M, Antl M, Huber B, Stoecker K, Ebrecht D, et al. (2003) Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cellular Microbiology 5: 343-351.
25. Springman AC, Jacobs JL, Somvanshi VS, Sundin GW, Mulks MH, et al. (2009) Genetic diversity and multihost pathogenicity of clinical and environmental strains of Burkholderia cenocepacia. Appl Environ Microbiol. pp AEM.00877-00809.
26. Rao AU, Carta LK, Lesuisse E, Hamza I (2005) Lack of heme synthesis in a free-living eukaryote. Proc Natl Acad Sci U S A 102: 4270-4275.
27. Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96: 47-56.
28. Tan MW, Mahajan-Miklos S, Ausubel FM (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96: 715-720.
29. Chen JS, Witzmann KA, Spilker T, Fink RJ, LiPuma JJ (2001) Endemicity and inter-city spread of Burkholderia cepacia genomovar III in cystic fibrosis. J Pediatr 139: 643-649.
30. Coenye T, Spilker T, Martin A, LiPuma JJ (2002) Comparative assessment of genotyping methods for epidemiologic study of Burkholderia cepacia genomovar III. J Clin Microbiol 40: 3300-3307.
31. Baldwin A, Mahenthiralingam E, Thickett KM, Honeybourne D, Maiden MC, et al. (2005) Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 43: 4665-4673.
32. Baldwin A, Mahenthiralingam E, Drevinek P, Pope C, Waine DJ, et al. (2008) Elucidating Global Epidemiology of Burkholderia multivorans in Cases of Cystic Fibrosis by Multilocus Sequence Typing. Journal of Clinical Microbiology 46: 290-295.
33. Coenye T, LiPuma JJ (2003) Population structure analysis of Burkholderia cepacia genomovar III: varying degrees of genetic recombination characterize major clonal complexes. Microbiology 149: 77-88.
34. LiPuma JJ, Spilker T, Gill LH, Campbell PW, Liu L, et al. (2001) Disproportionate distribution of Burkholderia cepacia complex species and transmissibility markers in cystic fibrosis. Am J Respir Crit Care Med 164: 92-96.
35. Huber B, Feldmann F, Kothe M, Vandamme P, Wopperer J, et al. (2004) Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans. Infect Immun 72: 7220-7230.
36. Gallagher LA, Manoil C (2001) Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. Journal of Bacteriology 183: 6207-6214.
37. Engledow AS, Medrano EG, Mahenthiralingam E, LiPuma JJ, Gonzalez CF (2004) Involvement of a plasmid-encoded type IV secretion system in the plant tissue watersoaking phenotype of Burkholderia cenocepacia. J Bacteriol 186: 6015-6024.
38. Yoder-Himes DR, Chain PSG, Zhu Y, Wurtzel O, Rubin EM, et al. (2009) Mapping the Burkholderia cenocepacia niche response via high-throughput sequencing. Proceedings of the National Academy of Sciences 106: 3976-3981.
39. Lewenza S, Sokol PA (2001) Regulation of ornibactin biosynthesis and N-acyl-L-homoserine lactone production by CepR in Burkholderia cepacia. Journal of Bacteriology 183: 2212-2218.
40. Bargmann CI (2006) Chemosensation in C. elegans. In: Wormbook, editor The Celegans Research Community, Wormbook.
41. Kurz CL, Ewbank JJ (2003) Caenorhabditis elegans: an emerging genetic model for the study of innate immunity. Nature Reviews Genetics 4: 380-390.
42. Kurz CL, Tan MW (2004) Regulation of aging and innate immunity in C. elegans. Aging Cell 3: 185-193.
43. Garvis S, Munder A, Ball G, de Bentzmann S, Wiehlmann L, et al. (2009) Caenorhabditis elegans Semi-Automated Liquid Screen Reveals a Specialized Role for the Chemotaxis Gene cheB2 in Pseudomonas aeruginosa Virulence. PLoS Pathog 5: e1000540.
44. Kidd TJ, Douglas JM, Bergh HA, Coulter C, Bell SC (2008) Burkholderia cepacia complex epidemiology in persons with cystic fibrosis from Australia and New Zealand. Research in Microbiology 159: 194-199.
45. Govan JR, Brown AR, Jones AM (2007) Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection. Future Microbiol 2: 153-164.
46. McDowell A, Mahenthiralingam E, Dunbar KEA, Moore JE, Crowe M, et al. (2004) Epidemiology of Burkholderia cepacia complex species recovered from cystic fibrosis patients: issues related to patient segregation. Journal of Medical Microbiology 53: 663-668.
47. Jones AM, Dodd ME, Govan JR, Barcus V, Doherty CJ, et al. (2004) Burkholderia cenocepacia and Burkholderia multivorans: influence on survival in cystic fibrosis. Thorax 59: 948-951.
48. Ledson MJ, Gallagher MJ, Jackson M, Hart CA, Walshaw MJ (2002) Outcome of Burkholderia cepacia colonisation in an adult cystic fibrosis centre. Thorax 57: 142-145.
49. McCloskey M, McCaughan J, Redmond AOB, Elborn JS (2001) Clinical outcome after acquisition of Burkholderia cepacia in patients with cystic fibrosis. Irish Journal of Medical Science 170: 28-31.
50. Uehlinger S, Schwager S, Bernier SP, Riedel K, Nguyen DT, et al. (2009) Identification of specific and universal virulence factors in Burkholderia cenocepacia strains using multiple infection hosts. Infect Immun.
51. D'Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Deziel E, et al. (2007) Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64: 512-533.
52. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, et al. (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Developmental Cell 7: 745-754.
53. Furukawa S, Kuchma SL, O'Toole GA (2006) Keeping their options open: Acute versus persistent infections. Journal of Bacteriology 188: 1211-1217.
54. Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, et al. (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci U S A 97: 8815-8821.
55. Caiazza NC, Merritt JH, Brothers KM, O'Toole GA (2007) Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189: 3603-3612.
56. Sulston J, Hodgkin J (1988) Methods. In: Wood WB, ed. The Nematode Caenorhabditis elegans: Cold Spring Harbor Press. pp 587-606.
57. Tomlin KL, Clark SR, Ceri H (2004) Green and red fluorescent protein vectors for use in biofilm studies of the intrinsically resistant Burkholderia cepacia complex. Journal of Microbiological Methods 57: 95-106.
58. Henry DA, Campbell ME, LiPuma JJ, Speert DP (1997) Identification of Burkholderia cepacia isolates from patients with cystic fibrosis and use of a simple new selective medium. J Clin Microbiol 35: 614-619.
59. Clegg ED, LaPenotiere HF, French DY, Szilagyi M (2002) Use of CeHR axenic medium for exposure and gene expression studies.
60. Choi K-H, DeShazer D, Schweizer HP (2006) Mini-Tn7 insertion in bacteria with multiple attTn7 sites: example Burkholderia mallei ATCC 23344. Nature Protocols 1: 162-169.
61. Birren BW, Lander ES, Galagan J, Devon K, Nusbaum C, et al. (2005) The genome sequence of Burkholderia cenocepacia PC184. Cambridge MA: The Broad Institute Genome Sequencing Platform.
62. Coenye T, Vandamme P, LiPuma JJ, Govan JRW, Mahenthiralingam E (2003) Updated version of the Burkholderia cepacia complex experimental strain panel. Journal of Clinical Microbiology 41: 2797-2798.