Effect of environmental stress factors on the uptake and survival of Campylobacter jejuni in Acanthamoeba castellanii

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Bui, Xuan Thanh ^a,b   Qvortrup, Klaus ^c   Wolff, Anders ^a   Bang, Dang Duong ^a   Creuzenet, Carole ^b  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Acanthamoeba castellanii; Campylobacter jejuni; Environmental stresses; Virulence

Indexed keywords

BACTERIAL PROTEIN; PROTEIN CIAB; PROTEIN DNAJ; PROTEIN HTRA; UNCLASSIFIED DRUG;

ACANTHAMOEBA CASTELLANII; AMOEBA (LIFE CYCLE STAGE); ARTICLE; BACTERIAL VIRULENCE; BACTERIUM CULTURE; CAMPYLOBACTER JEJUNI; CELL SURVIVAL; CELL VIABILITY; COLONY FORMING UNIT; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; GENETIC TRANSCRIPTION; HEAT STRESS; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION;

ACANTHAMOEBA CASTELLANII; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOT TEMPERATURE; MICROBIAL VIABILITY; OSMOTIC PRESSURE; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; VIRULENCE FACTORS;

ACANTHAMOEBA CASTELLANII; BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; PROTOZOA;

EID: 84867235633     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-232     Document Type: Article

References (62)

1. Infectious gastroenteritis and colitis diarrhea. Newton JM, Surawicz CM, Diarrhea, clinical gastroenterology New York: Humana Press, Guandalini S, Vaziri H, 2011 33 59
2. Source attribution of human campylobacteriosis using a meta-analysis of case-control studies of sporadic infections. Domingues AR, Pires SM, Halasa T, Hald T, Epidemiol Infect 2012 140 970 981 10.1017/S0950268811002676 22214729
3. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Beery JT, Hugdahl MB, Doyle MP, Appl Environ Microbiol 1988 54 2365 2370 3060015
4. Polyphosphate kinase 1 is a pathogenesis determinant in Campylobacter jejuni. Candon HL, Allan BJ, Fraley CD, Gaynor EC, J Bacteriol 2007 189 8099 8108 10.1128/JB.01037-07 17827292
5. Campylobacter jejuni infections in the United States and other industrialized nations. Friedman CR, Neimann J, Wegener HC, Tauxe RV, Campylobacter Washington, DC: ASM Press, Nachamkin I, vol. 2, 2 2000 121 138 MJB
6. Stress response and pathogenic potential of Campylobacter jejuni cells exposed to starvation. Klančnik A, Guzej B, Jamnik P, Vučković D, Abram M, Možina SS, Res Microbiol 2009 160 345 352 10.1016/j.resmic.2009.05.002 19477271
7. Survival mechanisms and culturability of Campylobacter jejuni under stress conditions. Jackson D, Davis B, Tirado S, Duggal M, van Frankenhuyzen J, Deaville D, Wijesinghe M, Tessaro M, Trevors J, Antonie van Leeuwenhoek 2009 96 377 394 10.1007/s10482-009-9378-8 19774483
8. Stress response of Campylobacter spp. and its role in food processing. Alter T, Scherer K, J Vet Med B Infect Dis Vet Public Health 2006 53 351 357 10.1111/j.1439-0450.2006.00983.x 17010037
9. Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. Fields JA, Thompson SA, J Bacteriol 2008 190 3411 3416 10.1128/JB.01928-07 18310331
10. Stress-induced adaptive tolerance response and virulence gene expression in Campylobacter jejuni. Ma Y, Hanning I, Slavik M, J Food Safety 2009 29 126 143 10.1111/j.1745-4565.2008.00147.x
11. Characterization of the thermal stress response of Campylobacter jejuni. Konkel ME, Kim BJ, Klena JD, Young CR, Ziprin R, Infect Immun 1998 66 3666 3672 9673247
12. Gene expression profile of Campylobacter jejuni in response to growth temperature variation. Stintzi A, J Bacteriol 2003 185 2009 2016 10.1128/JB.185.6.2009-2016.2003 12618466
13. The Campylobacter jejuni transcriptional regulator Cj1556 plays a role in the oxidative and aerobic stress response and is important for bacterial survival in vivo. Gundogdu O, Mills DC, Elmi A, Martin MJ, Wren BW, Dorrell N, J Bacteriol 2011 193 4238 4249 10.1128/JB.05189-11 21642451
14. A most probable number method for estimating small numbers of campylobacters in water. Bolton FJ, Hinchliffe PM, Coates D, Robertson L, J Hyg (Lond) 1982 89 185 190 10.1017/S0022172400070716
15. Evaluation of the effect of temperature and nutrients on the survival of Campylobacter spp. in water microcosms. Thomas C, Hill DJ, Mabey M, J Appl Microbiol 1999 86 1024 1032 10.1046/j.1365-2672.1999.00789.x 10389249
16. Culturability, injury and morphological dynamics of thermophilic Campylobacter spp. within a laboratory-based aquatic model system. Thomas C, Hill D, Mabey M, J Appl Microbiol 2002 92 433 442 10.1046/j.1365-2672.2002. 01550.x 11872118
17. Detection and typing of Campylobacter jejuni and Campylobacter coli and analysis of indicator organisms in three waterborne outbreaks in Finland. Hanninen M-L, Haajanen H, Pummi T, Wermundsen K, Katila M-L, Sarkkinen H, Miettinen I, Rautelin H, Appl Environ Microbiol 2003 69 1391 1396 10.1128/AEM.69.3.1391-1396.2003 12620821
18. Characterization of waterborne outbreak-associated Campylobacter jejuni, Walkerton, Ontario. Clark CG, Price L, Ahmed R, Woodward DL, Melito PL, Rodgers FG, Jamieson F, Ciebin B, Li A, Ellis A, Emerg Infect Dis 2003 9 1232 1241 10.3201/eid0910.020584 14609457
19. Comparison of free-living amoebae in hot water systems of hospitals with isolates from moist sanitary areas by identifying genera and determining temperature tolerance. Rohr U, Weber S, Michel R, Selenka F, Wilhelm M, Appl Environ Microbiol 1998 64 1822 1824 9572957
20. Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. Thomas V, Loret J-F, Jousset M, Greub G, Environ Microbiol 2008 10 2728 2745 10.1111/j.1462-2920.2008.01693.x 18637950
21. Free-living amoebae and their intracellular pathogenic microorganisms: risks for water quality. Thomas V, McDonnell G, Denyer SP, Maillard J-Y, FEMS Microbiol Rev 2010 34 231 259 10.1111/j.1574-6976.2009.00190.x 19744244
22. Mechanism involved in phagocytosis and killing of Listeria monocytogenes by Acanthamoeba polyphaga. Akya A, Pointon A, Thomas C, Parasitol Res 2009 105 1375 1383 10.1007/s00436-009-1565-z 19644706
23. Differential binding capacity and internalisation of bacterial substrates as factors in growth rate of Acanthamoeba spp. Bottone EJ, Pere AA, Gordon RE, Qureshi MN, J Med Microbiol 1994 40 148 154 10.1099/00222615-40-2-148 8107064
24. Amoebae and algae can prolong the survival of Campylobacter species in co-culture. Axelsson-Olsson D, Olofsson J, Svensson L, Griekspoor P, Waldenström J, Ellström P, Olsen B, Exp Parasitol 2010 126 59 64 10.1016/j.exppara.2009.12.016 20056117
25. Protozoan Acanthamoeba polyphaga as a potential reservoir for Campylobacter jejuni. Axelsson-Olsson D, Waldenstrom J, Broman T, Olsen B, Holmberg M, Appl Environ Microbiol 2005 71 987 992 10.1128/AEM.71.2.987-992.2005 15691957
26. Influence of temperature, oxygen and bacterial strain identity on the association of Campylobacter jejuni with Acanthamoeba castellanii. Baré J, Sabbe K, Huws S, Vercauteren D, Braeckmans K, Van Gremberghe I, Favoreel H, Houf K, FEMS Microbiol Ecol 2010 74 371 381 10.1111/j.1574-6941.2010.00955.x 20722733
27. Survival of Campylobacter jejuni in co-culture with Acanthamoeba castellanii: role of amoeba-mediated depletion of dissolved oxygen. Bui XT, Winding A, Qvortrup K, Wolff A, Bang DD, Creuzenet C, Environ Microbiol 2012 14 2034 2047 10.1111/j.1462-2920.2011.02655.x 22176643
28. Survival of Campylobacter jejuni in waterborne protozoa. Snelling WJ, McKenna JP, Lecky DM, Dooley JSG, Appl Environ Microbiol 2005 71 5560 5571 10.1128/AEM.71.9.5560-5571.2005 16151149
29. Colonization of broilers by Campylobacter jejuni internalized within Acanthamoeba castellanii. Snelling W, Stern N, Lowery C, Moore J, Gibbons E, Baker C, Dooley J, Arch Microbiol 2008 189 175 179 10.1007/s00203-007-0303-0 17882400
30. Induction of an adaptive tolerance response in the foodborne pathogen, Campylobacter jejuni. Murphy C, Carroll C, Jordan KN, FEMS Microbiol Let 2003 223 89 93 10.1016/S0378-1097(03)00348-3
31. Diversity and habitat specificity of free-living protozoa in commercial poultry houses. Baré J, Sabbe K, Van Wichelen J, van Gremberghe I, D'hondt S, Houf K, Appl Environ Microbiol 2009 75 1417 1426 10.1128/AEM.02346-08 19124593
32. Persistence of free-living protozoan communities across rearing cycles in commercial poultry houses. Baré J, Houf K, Verstraete T, Vaerewijck M, Sabbe K, Appl Environ Microbiol 2011 77 1763 1769 10.1128/AEM.01756-10 21239551
33. Increase in acid tolerance of Campylobacter jejuni through coincubation with amoebae. Axelsson-Olsson D, Svensson L, Olofsson J, Salomon P, Waldenström J, Ellström P, Olsen B, Appl Environ Microbiol 2010 76 4194 4200 10.1128/AEM.01219-09 20453130
34. Cytokine responses in primary chicken embryo intestinal cells infected with Campylobacter jejuni strains of human and chicken origin and the expression of bacterial virulence-associated genes. Li Y-P, Ingmer H, Madsen M, Bang D, BMC Microbiol 2008 8 107 10.1186/1471-2180-8-107 18588667
35. Bacterial secreted proteins are required for the internalization of Campylobacter jejuni into cultured mammalian cells. Konkel ME, Kim BJ, Rivera-Amill V, Garvis SG, Mol Microbiol 1999 32 691 701 10.1046/j.1365-2958. 1999.01376.x 10361274
36. Construction and characterization of a Yersinia enterocolitica O:8 high- temperature requirement (htrA) isogenic mutant. Li S, Dorrell N, Everest P, Dougan G, Wren B, Infect Immun 1996 64 2088 2094 8675311
37. Degradation by proteases Lon, Clp and HtrA, of Escherichia coli proteins aggregated in vivo by heat shock; HtrA protease action in vivo and in vitro. Laskowska E, Kuczyńska-Wiśnik D, Skórko-Glonek J, Taylor A, Mol Microbiol 1996 22 555 571 10.1046/j.1365-2958.1996.1231493.x 8939438
38. Role of Campylobacter jejuni potential virulence genes in cecal colonization. Ziprin RL, Young CR, Byrd JA, Stanker LH, Hume ME, Gray SA, Kim BJ, Konkel ME, Avian Dis 2001 45 549 557 10.2307/1592894 11569726
39. The HtrA protease of Campylobacter jejuni is required for heat and oxygen tolerance and for optimal interaction with human epithelial cells. Brondsted L, Andersen MT, Parker M, Jorgensen K, Ingmer H, Appl Environ Microbiol 2005 71 3205 3212 10.1128/AEM.71.6.3205-3212.2005 15933023
40. Environmental survival mechanisms of the foodborne pathogen Campylobacter jejuni. Murphy C, Carroll C, Jordan KN, J Appl Microbiol 2006 100 623 632 10.1111/j.1365-2672.2006.02903.x 16553716
41. High hydrostatic pressure resistance of Campylobacter jejuni after different sublethal stresses. Sagarzazu N, Cebrián G, Condón S, Mackey B, Mañas P, J Appl Microbiol 2010 109 146 155 20028438
42. Campylobacter jejuni contains two Fur homologs: Characterization of iron-responsive regulation of peroxide stress defense genes by the PerR repressor. van Vliet AHM, Baillon M-LA, Penn CW, Ketley JM, J Bacteriol 1999 181 6371 6376 10515927
43. Campylobacter jejuni: molecular biology and pathogenesis. Young KT, Davis LM, DiRita VJ, Nat Rev Micro 2007 5 665 679 10.1038/nrmicro1718
44. Recovery in embryonated eggs of viable but nonculturable Campylobacter jejuni cells and maintenance of ability to adhere to HeLa cells after resuscitation. Cappelier JM, Minet J, Magras C, Colwell RR, Federighi M, Appl Environ Microbiol 1999 65 5154 5157 10543837
45. Environmental stress factors affecting survival and virulence of Campylobacter jejuni. Mihaljevic RR, Sikic M, Klancnik A, Brumini G, Mozina SS, Abram M, Microb Pathog 2007 43 120 125 10.1016/j.micpath.2007.03.004 17512161
46. Polyphosphate kinase 2: A novel determinant of stress responses and pathogenesis in Campylobacter jejuni. Gangaiah D, Liu Z, Arcos J, Kassem II, Sanad Y, Torrelles JB, Rajashekara G, PLoS One 2010 5 12142 10.1371/journal. pone.0012142 20808906
47. Attachment, invasion, and translocation of Campylobacter jejuni in pig small-intestinal epithelial cells. Pogačar MŠ Klančnik A, Možina SS, Cencič A, Foodborne Pathog Dis 2009 7 589 595
48. Effect of low-osmolality nutrient media on growth and culturability of Campylobacter species. Reezal A, McNeil B, Anderson JG, Appl Environ Microbiol 1998 64 4643 4649 9835543
49. Survival and stress induced expression of groEL and rpoD of Campylobacter jejuni from different growth phases. Klančnik A, Botteldoorn N, Herman L, Možina SS, Int J Food Microbiol 2006 112 200 207 10.1016/j. ijfoodmicro.2006.03.015 16782221
50. Characterization of the oxidative stress stimulon and PerR regulon of Campylobacter jejuni. Palyada K, Sun Y-Q, Flint A, Butcher J, Naikare H, Stintzi A, BMC Genomics 2009 10 481 10.1186/1471-2164-10-481 19835633
51. Environmental signals controlling expression of virulence determinants in bacteria. Mekalanos JJ, J Bacteriol 1992 174 1 7 1729202
52. Microbial stress response in minimal processing. Abee T, Wouters JA, Int J Food Microbiol 1999 50 65 91 10.1016/S0168-1605(99)00078-1 10488845
53. Examination of stress and virulence gene expression in Escherichia coli O157:H7 using targeted microarray analysis. Allen KJ, Lepp D, McKellar RC, Griffiths MW, Foodborne Pathog Dis 2008 5 437 447 10.1089/fpd.2008.0100 18713062
54. Culture of Campylobacter jejuni with sodium deoxycholate induces virulence gene expression. Malik-Kale P, Parker CT, Konkel ME, J Bacteriol 2008 190 2286 2297 10.1128/JB.01736-07 18223090
55. HtrA chaperone activity contributes to host cell binding in Campylobacter jejuni. Baek K, Vegge C, Brondsted L, Gut Pathog 2011 3 13 10.1186/1757-4749-3- 13 21939552
56. Different contributions of HtrA protease and chaperone activities to Campylobacter jejuni stress tolerance and physiology. Baek KT, Vegge CS, Skorko-Glonek J, Brondsted L, Appl Environ Microbiol 2011 77 57 66 10.1128/AEM.01603-10 21075890
57. Insect infection model for Campylobacter jejuni reveals that O-methyl phosphoramidate has insecticidal activity. Champion OL, Karlyshev AV, Senior NJ, Woodward M, La Ragione R, Howard SL, Wren BW, Titball RW, J Infect Dis 2010 201 776 782 20113177
58. Survival of stress exposed Campylobacter jejuni in the murine macrophage J774 cell line. Pogačar MŠ Roberta RM, Anja K, Gordana B, Maja A, Sonja SM, Int J Food Microbiol 2009 129 68 73 10.1016/j.ijfoodmicro.2008.11.010 19058868
59. Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii. Oelschlaeger TA, Guerry P, Kopecko DJ, Proc Natl Acad Sci U S A 1993 90 6884 6888 10.1073/pnas.90.14.6884 8341714
60. A quantitative model of intracellular growth of Legionella pneumophila in Acanthamoeba castellanii. Moffat JF, Tompkins LS, Infect Immun 1992 60 296 301 1729191
61. Reverse transcriptase real-time PCR for detection and quantification of viable Campylobacter jejuni directly from poultry faecal samples. Bui XT, Wolff A, Madsen M, Bang DD, Res Microbiol 2012 163 64 72 10.1016/j.resmic.2011.10.007 22064380
62. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Livak KJ, Schmittgen TD, Methods 2001 25 402 408 10.1006/meth.2001.1262 11846609