Polymorphisms in rpos and Stress Tolerance Heterogeneity in Natural Isolates of Cronobacter sakazakii

Applied and Environmental Microbiology

Volumn 78, Issue 11, 2012, Pages 3975-3984

  Álvarez Ordóñez, Avelino ^a,b   Begley, Máire ^a   Hill, Colin ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

A-CARBON; CATALASE ACTIVITY; COMPLEMENTATION; FOOD CHAIN; HEAT STRESS; HIGH VARIABILITY; OXIDATIVE TREATMENT; PHENOTYPIC DIVERSITY; STRESS CONDITION; STRESS TOLERANCE;

OSMOSIS;

GENES;

ACETIC ACID DERIVATIVE; BACTERIAL PROTEIN; CAROTENOID; CATALASE; SIGMA FACTOR; SIGMA FACTOR KATF PROTEIN, BACTERIA;

ADAPTATION; BACTERIUM; CAROTENOID; ENVIRONMENTAL STRESS; FOOD CHAIN; HETEROGENEITY; OXIDATION; PHENOTYPIC PLASTICITY; POLYMORPHISM; TOLERANCE;

ANIMAL; ARTICLE; ARTIFICIAL MILK; CRONOBACTER SAKAZAKII; ENTEROBACTERIACEAE INFECTION; FOOD CONTROL; GENETIC POLYMORPHISM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MILK; NEWBORN; OSMOTIC PRESSURE; OXIDATIVE STRESS; PH; PHYSIOLOGY;

ACETATES; ANIMALS; BACTERIAL PROTEINS; CAROTENOIDS; CATALASE; CRONOBACTER SAKAZAKII; ENTEROBACTERIACEAE INFECTIONS; FOOD MICROBIOLOGY; HEAT-SHOCK RESPONSE; HUMANS; HYDROGEN-ION CONCENTRATION; INFANT FORMULA; INFANT, NEWBORN; MILK; OSMOTIC PRESSURE; OXIDATIVE STRESS; POLYMORPHISM, GENETIC; SIGMA FACTOR;

BACTERIA (MICROORGANISMS);

EID: 84864084414     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.07835-11     Document Type: Article

References (59)

1. Adekunte A, et al. 2010. Resistance of Cronobacter sakazakii in reconstituted powdered infant formula during ultrasound at controlled temperatures: a quantitative approach on microbial responses. Int. J. Food Microbiol. 142:53-59.
2. Al-Holy MA, Lin M, Abu-Ghoush MM, Al-Qadiri HM, Rasco BA. 2009. Thermal resistance, survival and inactivation of Enterobacter sakazakii (Cronobacter spp.) in powdered and reconstituted infant formula. J. Food Saf. 29:287-301.
3. Arroyo C, Condón S, Pagán R. 2009. Thermobacteriological characterization of Enterobacter sakazakii. Int. J. Food Microbiol. 136:110 -118.
4. Arroyo C, Cebrián G, Pagán R, Condón S. 2010. Resistance of Enterobacter sakazakii to pulsed electric fields. Innov. Food Sci. Emerg. 11:314-321.
5. Benito A, Ventoura G, Casadei M, Robinson T, Mackey B. 1999. Variation in resistance of natural isolates of Escherichia coli O157 to high hydrostatic pressure, mild heat and other stresses. Appl. Environ. Microbiol. 65:1564 -1569.
6. Besse NG, Leclercq A, Maladen V, Tyburski C, Lombard B. 2006. Evaluation of the International Organization for Standardization-International Dairy Federation (ISO-IDF) draft standard method for detection of Enterobacter sakazakii in powered infant formulas. J. AOAC Int. 89:1309-1316.
7. Beuchat LR, et al. 2009. Cronobacter sakazakii in foods and factors affecting its survival, growth and inactivation. Int. J. Food Microbiol. 136:204-213.
8. Bhagwat AA, et al. 2005. Characterization of enterohemorrhagic Escherichia coli strains based on acid resistance phenotypes. Infect. Immun. 73:4993-5003.
9. Bhagwat AA, et al. 2006. Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Appl. Environ. Microbiol. 72:4978-4986.
10. Biesta-Peters EG, Reij MW, Joosten H, Gorris LGM, Zwietering MH. 2010. Comparison of two optical-density-based methods and a plate count method for estimation of growth parameters of Bacillus cereus. Appl. Environ. Microbiol. 76:1399 -1405.
11. Breeuwer P, Lardeau A, Peterz M, Joosten HM. 2003. Desiccation and heat tolerance of Enterobacter sakazakii. J. Appl. Microbiol. 95:967-973.
12. Cawthorn DM, Botha S, Witthuhn RC. 2008. Evaluation of different methods for the detection and identification of Enterobacter sakazakii isolated from South African infant formula milks and the processing environment. Int. J. Food Microbiol. 127:129 -138.
13. Chenu JW, Cox JM. 2009. Cronobacter (" Enterobacter sakazakii" ): current status and future prospects. Lett. Appl. Microbiol. 49:153-159.
14. Chiang SM, Dong T, Edge TA, Schellhorn HE. 2011. Phenotypic diversity caused by differential RpoS activity among environmental Escherichia coli isolates. Appl. Environ. Microbiol. 77:7915-7923.
15. Culham DE, Wood JM. 2000. An Escherichia coli reference collection group B2- and uropathogen-associated polymorphism in the rpoS-mutS region of the E. coli chromosome. J. Bacteriol. 182:6272- 6276.
16. Dancer GI, Mah JH, Rhee MS, Hwang IG, Kang DH. 2009. Resistance of Enterobacter sakazakii (Cronobacter spp.) to environmental stresses. J. Appl. Microbiol. 107:1606 -1614.
17. den Besten HMW, et al. 2010. Short- and long-term biomarkers for bacterial robustness: a framework for quantifying correlations between cellular indicators and adaptive behavior. PLoS One 5:e13746.
18. Dodd CER, Aldsworth TG. 2002. The importance of RpoS in the survival of bacteria through food processing. Int. J. Food Microbiol. 74:189 -194.
19. Dong T, Schellhorn HE. 2010. Role of RpoS in virulence of pathogens. Infect. Immun. 78:887- 897.
20. Dong T, Chiang SM, Joyce C, Yu R, Schellhorn HE. 2009. Polymorphism and selection of rpoS in pathogenic Escherichia coli. BMC Microbiol. 9:118.
21. Edelson-Mammel S, Porteous MK, Buchanan RL. 2006. Acid resistance of twelve strains of Enterobacter sakazakii, and the impact of habituating the cells to an acidic environment. J. Food Sci. 71:M201-M207.
22. Farber JM. 2004. Enterobacter sakazakii: new foods for thought? Lancet 363:5- 6.
23. Farrell MJ, Finkel SE. 2003. The growth advantage in stationary-phase phenotype conferred by rpoS mutations is dependent on the pH and nutrient environment. J. Bacteriol. 185:7044 -7052.
24. Ferenci T. 2003. What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? Trends Microbiol. 11:457- 461.
25. Ferenci T. 2008. The spread of a beneficial mutation in experimental bacterial populations: the influence of the environment and genotype of the fixation of rpoS mutations. Heredity 100:446-452.
26. Ferenci T, Spira B. 2007. Variation in stress responses within a bacterial species and the indirect costs of stress resistance. Ann. N. Y. Acad. Sci. 1113:105-113.
27. Finkel SE, Kolter R. 1999. Evolution of microbial diversity during prolonged starvation. Proc. Natl. Acad. Sci. U. S. A. 96:4023- 4027.
28. Friedemann M. 2007. Enterobacter sakazakii in food and beverages (other than infant formula and milk powder). Int. J. Food Microbiol. 116:1-10.
29. Gruszecki WI, Strzalka K. 2005. Carotenoids as modulators of lipid membrane physical properties. Biochim. Biophys. Acta 1740:108 -115.
30. Gurtler JB, Kornacki JL, Beuchat LR. 2005. Enterobacter sakazakii: a coliform of increased concern to infant health. Int. J. Food Microbiol. 104:1-34.
31. Hauben KJA, et al. 1997. Escherichia coli mutants resistant to inactivation by high hydrostatic pressure. Appl. Environ. Microbiol. 63:945-950.
32. Healy B, et al. 2010. Cronobacter (Enterobacter sakazakii): an opportunistic foodborne pathogen. Foodborne Pathog. Dis. 7:339 -350.
33. Hengge-Aronis R. 2000. The general stress response in Escherichia coli, p 161-178. In Storz G, Hengge-Aronis R (ed), Bacterial stress responses. ASM Press, Washington, DC.
34. Humphrey TJ, Slater E, McAlpine K, Rowbury RJ, Gilbert R. 1995. Salmonella enteritidis phage type 4 isolates more tolerant of heat, acid, or hydrogen peroxide also survive longer on surfaces. Appl. Environ. Microbiol. 61:3161-3164.
35. Iversen C, Forsythe S. 2003. Risk profile for Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci. Technol. 14:443- 454.
36. Iversen C, et al. 2007. Identification of "Cronobacter" spp. (Enterobacter sakazakii). J. Clin. Microbiol. 45:3814 -3816.
37. Johler S, Stephan R, Hartmann I, Kuehner KA, Lehner A. 2010. Genes involved in yellow pigmentation of Cronobacter sakazakii ES5 and influence of pigmentation on persistence and growth under environmental stress. Appl. Environ. Microbiol. 76:1053-1061.
38. King T, Ishihama A, Kori A, Ferenci T. 2004. A regulatory trade-off as a source of strain variation in the species Escherichia coli. J. Bacteriol. 186: 5614-5620.
39. Lai KK. 2001. Enterobacter sakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature. Medicine (Baltimore) 80:113-122.
40. Large TM, Walk ST, Whittam TS. 2005. Variation in acid resistance among Shiga toxin-producing clones of pathogenic Escherichia coli. Appl. Environ. Microbiol. 71:2493-2500.
41. Lehner A, et al. 2006. Cloning and characterization of Enterobacter sakazakii pigment genes and in situ spectroscopic analysis of the pigment. FEMS Microbiol. Lett. 265:244 -248.
42. Lodato P, et al. 2007. Expression of the carotenoid biosynthesis genes in Xanthophyllomyces dendrorhous. Biol. Res. 40:73- 84.
43. McGrath S, Fitzgerald GF, van Sinderen D. 2001. Improvement and optimization of two engineered phage resistance mechanisms in Lactococcus lactis. Appl. Environ. Microbiol. 67:608-616.
44. Morikawa K, et al. 2001. Overexpression of sigma factor, _B, urges Staphylococcus aureus to thicken the cell wall and to resist -lactams. Biochem. Biophys. Res. Commun. 288:385-389.
45. Morrissey R, et al. 2011. Real-time monitoring of luciferase-tagged Cronobacter sakazakii in reconstituted infant milk formula. J. Food Prot. 74:573-579.
46. Mullane NR, et al. 2007. Enterobacter sakazakii an emerging bacterial pathogen with implications for infant health. Minerva Pediatr. 59:137-148.
47. Navarro Llorens JM, Tormo A, Martínez-García E. 2010. Stationary phase in gram-negative bacteria. FEMS Microbiol. Rev. 34:476-495.
48. Notley-McRobb L, King T, Ferenci T. 2002. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J. Bacteriol. 184:806-811.
49. Osaili T, Forsythe S. 2009. Desiccation resistance and persistence of Cronobacter species in infant formula. Int. J. Food Microbiol. 136:214-220.
50. Pérez MCP, Aliaga DR, Bernat CF, Enguidanos MR, López AM. 2007. Inactivation of Enterobacter sakazakii by pulsed electric field in buffered peptone water and infant formula milk. Int. Dairy J. 17:1441-1449.
51. Robbe-Saule V, Algorta G, Rouilhac I, Norel F. 2003. Characterization of the RpoS status of clinical isolates of Salmonella enterica. Appl. Environ. Microbiol. 69:4352- 4358.
52. Robey M, et al. 2001. Variation in resistance to high hydrostatic pressure and rpoS heterogeneity in natural isolates of Escherichia coli O157:H7. Appl. Environ. Microbiol. 67:4901- 4907.
53. Sedkova N, Tao L, Rouviere PE, Cheng Q. 2005. Diversity of carotenoid synthesis clusters from environmental Enterobacteriaceae strains. Appl. Environ. Microbiol. 71:8141- 8146.
54. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673- 4680.
55. Uhlich GA, Sinclair JR, Warren NG, Chmielecki WA, Fratamico P. 2008. Characterization of Shiga toxin-producing Escherichia coli isolates associated with two multistate food-borne outbreaks that occurred in 2006. Appl. Environ. Microbiol. 74:1268 -1272.
56. Waterman SR, Small PLC. 1996. Characterization of the acid resistance phenotype and rpoS alleles of Shiga-like toxin-producing Escherichia coli. Infect. Immun. 64:2808 -2811.
57. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: _S-dependent genes, promoters, and _ factor selectivity. J. Bacteriol. 187:1591-1603.
58. Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R. 1993. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757-1760.
59. Ziegelhoffer EC, Donohue TJ. 2009. Bacterial responses to photooxidative stress. Nat. Rev. Microbiol. 7:856-863.