Impact of Pathogen Population Heterogeneity and Stress-Resistant Variants on Food Safety

Annual Review of Food Science and Technology

Volumn 7, Issue , 2016, Pages 439-456

  Abee, T ^a   Koomen, J ^a   Metselaar, K I ^a   Zwietering, M H ^a   Den Besten, H M W ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Food processing; Growth kinetics; Listeria monocytogenes; Systems biology

Indexed keywords

DISEASES; FOOD PROCESSING; FOOD SAFETY; GROWTH KINETICS; KINETICS; LISTERIA; PATHOGENS; PROCESSED FOODS;

INACTIVATION KINETICS; LISTERIA MONOCYTOGENES; MOLECULAR MECHANISM; PATHOGEN POPULATIONS; PHENOTYPIC FEATURES; PROCESSING ENVIRONMENTS; SYSTEMS BIOLOGY; WHOLE GENOME SEQUENCES;

FOOD MICROBIOLOGY;

BIOLOGICAL MODEL; CLASSIFICATION; DEVICES; FOOD CONTROL; FOOD HANDLING; FOOD SAFETY; FOODBORNE DISEASES; GENETICS; GENOTYPE; HUMAN; LISTERIA MONOCYTOGENES; MICROBIOLOGY; MUTATION; PHENOTYPE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROCEDURES;

FOOD HANDLING; FOOD MICROBIOLOGY; FOOD SAFETY; FOODBORNE DISEASES; GENOTYPE; HUMANS; LISTERIA MONOCYTOGENES; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; STRESS, PHYSIOLOGICAL;

EID: 84959893807     PISSN: 19411413     EISSN: 19411421     Source Type: Journal    
DOI: 10.1146/annurev-food-041715-033128     Document Type: Review

References (73)

1. Abee T, Wels M, de Been M, den Besten H. 2011. From transcriptional landscapes to the identification of biomarkers for robustness. Microb. Cell Fact. 10(Suppl. 1):S9
2. Akanuma G, Nanamiya H, Natori Y, Yano K, Suzuki S, et al. 2012. Inactivation of ribosomal protein genes in Bacillus subtilis reveals importance of each ribosomal protein for cell proliferation and cell differentiation. J. Bacteriol. 194:6282-91
3. Amato SM, Fazen CH, Henry TC, Mok WW, Orman MA, et al. 2014. The role of metabolism in bacterial persistence. Front. Microbiol. 5:70
4. Aryani DC, den Besten HMW, HazelegerWC, Zwietering MH. 2015. Quantifying variability and the effect of growth history on thermal resistance of Listeria monocytogenes. Int. J. Food Microbiol. 193:130-38
5. Avery SV. 2006. Microbial cell individuality and the underlying sources of heterogeneity. Nat. Rev. Microbiol. 4(8):577-87
6. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. 2004. Bacterial persistence as a phenotypic switch. Science 305(5690):1622-25
7. Begley M, Hill C. 2015. Stress adaptation in foodborne pathogens. Annu. Rev. Food Sci. Technol. 6:191-210
8. Bergholz TM, Moreno Switt A, Wiedmann M. 2014. Omics approaches in food safety: fulfilling the promise? Trends Microbiol. 22(5):275-81
9. Booth I. 2002. Stress and the single cell: Intrapopulation diversity is a mechanism to ensure survival upon exposure to stress. Int. J. Food Microbiol. 78:19-30
10. Cabrita P, Trigo MJ, Ferreira RB, Brito L. 2015. Differences in the expression of cold stress-related genes and in the swarming motility among persistent and sporadic strains of Listeria monocytogenes. Foodborne Pathog. Dis. 12(7):576-84
11. Carpentier B, Cerf O. 2011. Persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 145(1):1-8
12. Cerf O. 1977. Tailing of survival curves of bacterial spores. J. Appl. Bacteriol. 42(1):1-19
13. Chick H. 1908. An investigation of the laws of disinfection. J. Hyg. 8:92-158
14. Coroller L, Leguerinel I, Mettler E, Savy N, Mafart P. 2006. General model, based on two mixed Weibull distributions of bacterial resistance, for describing various shapes of inactivation curves. Appl. Environ. Microbiol. 72(10):6493-502
15. Cotter PD, O'Reilly K, Hill C. 2001. Role of the glutamate decarboxylase acid resistance system in the survival of Listeria monocytogenes LO28 in low pH foods. J. Food Prot. 64:1362-68
16. den Besten HMW, Mataragas M, Moezelaar R, Abee T, Zwietering MH. 2006. Quantification of the effects of salt stress and physiological state on thermotolerance of Bacillus cereus ATCC 10987 and ATCC 14579. Appl. Environ. Microbiol. 72(9):5884-94
17. Durack J, Ross T, Bowman JP. 2013. Characterisation of the transcriptomes of genetically diverse Listeria monocytogenes exposed to hyperosmotic and low temperature conditions reveal global stress-adaptation mechanisms. PLOS ONE 8:e73603
18. FerreiraV, WiedmannM, Teixeira P, Stasiewicz MJ. 2014. Listeria monocytogenes persistence in food-associated environments: epidemiology, strain characteristics, and implications for public health. J. Food Prot. 77(1):150-70
19. Fox EM, Leonard N, Jordan K. 2011. Physiological and transcriptional characterization of persistent and nonpersistent Listeria monocytogenes isolates. Appl. Environ. Microbiol. 77(18):6559-69
20. Geeraerd AH, Herremans CH, Van Impe JF. 2000. Structural model requirements to describe microbial inactivation during a mild heat treatment. Int. J. Food Microbiol. 59:185-209
21. Geeraerd AH, ValdramidisVP, Van Impe JF. 2005. GInaFiT, a freeware tool to assess non-log-linearmicrobial survivor curves. Int. J. Food Microbiol. 102:95-105
22. Geeraerd AH, ValdramidisVP, Van Impe JF. 2005. GInaFiT, a freeware tool to assess non-log-linearmicrobial survivor curves. Int. J. Food Microbiol. 102:95-105.
23. Erratum. 2006. Int. J. Food Microbiol. 110:297
24. Germain E, Castro-Roa D, Zenkin N, Gerdes K. 2013. Molecular mechanism of bacterial persistence by HipA. Mol. Cell 52(2):248-54
25. Goeders N, Van Melderen L. 2014. Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6(1):304-24
26. Hein I, Klinger S, Dooms M, Flekna G, Stessl B, et al. 2011. Stress survival islet 1 (SSI-1) survey in Listeria monocytogenes reveals an insert common to Listeria innocua in sequence type 121 L. monocytogenes strains. Appl. Environ. Microbiol. 77(6):2169-73
27. Helaine S, Kugelberg E. 2014. Bacterial persisters: formation, eradication, and experimental systems. Trends Microbiol. 22(7):417-24
28. Holch A, Webb K, Lukjancenko O, Ussery D, Rosenthal BM, Gram L. 2013. Genome sequencing identifies two nearly unchanged strains of persistent Listeria monocytogenes isolated at two different fish processing plants sampled 6 years apart. Appl. Environ. Microbiol. 79(9):2944-51
29. Ivy RA, Wiedmann M, Boor KJ. 2012. Listeria monocytogenes grown at 7C shows reduced acid survival and an altered transcriptional response to acid shock compared to L. monocytogenes grown at 37C. Appl. Environ. Microbiol. 78(11):3824-36
30. Karatzas KA, BennikMH. 2002. Characterization of a Listeria monocytogenes Scott A isolate with high tolerance towards high hydrostatic pressure. Appl. Environ. Microbiol. 68(7):3183-89
31. Karatzas KA, Suur L, O'Byrne CP. 2012. Characterization of the intracellular glutamate decarboxylase system: analysis of its function, transcription, and role in the acid resistance of various strains of Listeria monocytogenes. Appl. Environ. Microbiol. 78(10):3571-79
32. Karatzas KA, Wouters JA, Gahan CG, Hill C, Abee T, Bennik MH. 2003. The CtsR regulator of Listeria monocytogenes contains a variant glycine repeat region that affects piezotolerance, stress resistance, motility and virulence. Mol. Microbiol. 49(5):1227-38
33. Karatzas KA, Valdramidis VP, Wells-Bennik MH. 2005. Contingency locus in ctsR of Listeria monocytogenes Scott A: a strategy for occurrence of abundant piezotolerant isolates within clonal populations. Appl. Environ. Microbiol. 71(12):8390-96
34. Kastbjerg VG, Hein-Kristensen L, Gram L. 2014. Triclosan-induced aminoglycoside-tolerant Listeria monocytogenes isolates can appear as small-colony variants. Antimicrob. Agents Chemother. 58(6):3124-32
35. Lewis K. 2012. Persister cells. Annu. Rev. Microbiol. 64:357-72
36. Mafart P, CouvertO, Gaillard S, Leguerinel I. 2002. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. Int. J. Food Microbiol. 72:107-13
37. Maisonneuve E, Gerdes K. 2014. Molecular mechanisms underlying bacterial persisters. Cell 157(3):539-48
38. Malley TJ, Butts J, Wiedmann M. 2015. Seek and destroy process: Listeria monocytogenes process controls in the ready-to-eat meat and poultry industry. J. Food Prot. 78(2):436-45
39. Metselaar KI, den Besten HMW, Abee T, Moezelaar R, Zwietering MH. 2013. Isolation and quantification of highly resistant variants of Listeria monocytogenes. Int. J. Food Microbiol. 166:508-14
40. Metselaar KI, den Besten HMW, Boekhorst J, Van Hijum SAFT, Zwietering MH, Abee T. 2015a. Diversity of acid stress resistant variants of Listeria monocytogenes and the potential role of ribosomal protein S21 encoded by rpsU. Front. Microbiol. 8(6):422
41. Metselaar KI, Saá Ibusquiza P, Ortiz Camargo AR, Krieg M, Zwietering MH, et al. 2015b. Performance of stress resistant variants of Listeria monocytogenes in mixed species biofilms with Lactobacillus plantarum. Int. J. Food Microbiol. 213:24-30
42. Mols M, Abee T. 2011. Bacillus cereus responses to acid stress. Environ. Microbiol. (11):2835-43
43. Müller A, Rychli K, Muhterem-Uyar M, Zaiser A, Stessl B, et al. 2013. Tn6188: a novel transposon in Listeria monocytogenes responsible for tolerance to benzalkonium chloride. PLOS ONE 8(10):e76835
44. Ochiai Y, Yamada F, Mochizuki M, Takano T, Hondo R, Ueda F. 2015. Biofilm formation under different temperature conditions by a single genotype of persistent Listeria monocytogenes strains. J. Food Prot. 77(1):133-40
45. O'Connell KP, Thomashow MF. 2000. Transcriptional organization and regulation of a polycistronic cold shock operon in Sinorhizobium meliloti RM1021 encoding homologs of the Escherichia coli major cold shock gene cspA and ribosomal protein gene rpsU. Appl. Environ. Microbiol. 66(1):392-400
46. Ortiz S, López V, Martínez-Suárez JV. 2014. Control of Listeria monocytogenes contamination in an Iberian pork processing plant and selection of benzalkonium chloride-resistant strains. Food Microbiol. 39:81-88
47. Patchett RA, Watson N, Fernandez PS, Kroll RG. 1996. The effect of temperature and growth rate on the susceptibility of Listeria monocytogenes to environmental stress conditions. Lett. Appl. Microbiol. 22:121-24
48. PelegM, Cole MB. 1998. Reinterpretation of microbial survival curves. Crit. Rev. Food Sci. Nutr. 38(5):353-80
49. Phan K, Ferenci T. 2013. A design-constraint trade-off underpins the diversity in ecologically important traits in species Escherichia coli. ISME J. 7:2034-43
50. Prax M, Bertram R. 2014. Metabolic aspects of bacterial persisters. Front. Cell. Infect. Microbiol. 22(4):148
51. Rajkovic A, Smigic N, Uyttendaele M, Medic H, de Zutter L, Devlieghere F. 2009. Resistance of Listeria monocytogenes, Escherichia coli O157:H7 and Campylobacter jejuni after exposure to repetitive cycles of mild bactericidal treatments. Food Microbiol. 26(8):889-95
52. Ramisetty BC, Natarajan B, Santhosh RS. 2015. mazEF-mediated programmed cell death in bacteria: "What is this" Crit. Rev. Microbiol. 41(1):89-100
53. Ryall B, Eydallin G, FerenciT. 2012. Culture history and population heterogeneity as determinants of bacterial adaptation: the adaptomics of a single environmental transition. Microbiol. Mol. Biol. Rev. 76(3):597-625
54. Sato N, Tachikawa T, Wada A, Tanaka A. 1997. Temperature-dependent regulation of the ribosomal smallsubunit protein S21 in the cyanobacterium Anabaena variabilis M3. J. Bacteriol. 179:7063-71
55. Schmitz-Esser S, Müller A, Stessl B, Wagner M. 2015. Genomes of sequence type 121 Listeria monocytogenes strains harbor highly conserved plasmids and prophages. Front. Microbiol. 28(6):380
56. Stasiewicz MJ, Oliver HF, Wiedmann M, den Bakker HC. 2015. Whole genome sequencing allows for improved identification of persistent Listeria monocytogenes in food associated environments. Appl. Environ. Microbiol. 81:6024-37
57. Stessl B, Fricker M, FoxE, KarpiskovaR, Demnerova K, et al. 2014. Collaborative survey on the colonization of different types of cheese-processing facilities with Listeria monocytogenes. Foodborne Pathog. Dis. 11(1):8-14
58. Stumbo CR. 1973. Thermal Bacteriology in Food Processing. New York: Academic
59. Takada H, Morita M, Shiwa Y, Sugimoto R, Suzuki S, et al. 2014. Cell motility and biofilm formation in Bacillus subtilis are affected by the ribosomal proteins, S11 and S21. Biosci. Biotechnol. Biochem. 78(5):898-907
60. Van Boeijen IKH, Casey PG, Hill C, Moezelaar R, Zwietering MH, et al. 2013. Virulence aspects of Listeria monocytogenes LO28 high pressure-resistant variants. Microb. Pathog. 59-60:48-51
61. Van Boeijen IKH, Chavaroche AAE, Valderrama WB, Moezelaar R, Zwietering MH, Abee T. 2010. Population diversity of Listeria monocytogenes LO28: phenotypic and genotypic characterization of variants resistant to high hydrostatic pressure. Appl. Environ. Microbiol. 76(7):2225-33
62. Van Boeijen IKH, Francke C, Moezelaar R, Abee T, Zwietering MH. 2011. Isolation of highly heat-resistant Listeria monocytogenes variants by use of a kinetic modeling-based sampling scheme. Appl. Environ. Microbiol. 77(8):2617-24
63. Van Boeijen IKH, Moezelaar R, Abee T, Zwietering MH. 2008. Inactivation kinetics of three Listeria monocytogenes strains under high hydrostatic pressure. J. Food Prot. 71(10):2007-13
64. Van Boekel MAJS. 2002. On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells. Int. J. Food Microbiol. 74:139-59
65. van der Veen S, Abee T. 2011. Bacterial SOS response: a food safety perspective. Curr. Opin. Biotechnol. 22(2):136-42
66. van der Veen S, van Schalkwijk S, Molenaar D, de Vos WM, Abee T, Wells-Bennik MH. 2010. The SOS response of Listeria monocytogenes is involved in stress resistance andmutagenesis. Microbiology 156:374-84
67. Vanlint D, Rutten N, Michiels CW, Aertsen A. 2012. Emergence and stability of high-pressure resistance in different food-borne pathogens. Appl. Environ. Microbiol. 78(9):3234-41
68. Van Melderen L. 2010. Toxin-antitoxin systems: why so many, what for? Curr. Opin. Microbiol. 13(6):781-85
69. Veening JW, SmitsWK, Kuipers OP. 2008. Bistability, epigenetics, and bet-hedging in bacteria. Annu. Rev. Microbiol. 62:193-210
70. Verghese B, Lok M, Wen J, Alessandria V, Chen Y, et al. 2011. ComK prophage junction fragments as markers for Listeria monocytogenes genotypes unique to individual meat and poultry processing plants and a model for rapid niche-specific adaptation, biofilm formation, and persistence. Appl. Environ. Microbiol. 77(10):3279-92
71. Vongkamjan K, Roof S, Stasiewicz MJ, WiedmannM. 2013. Persistent Listeria monocytogenes subtypes isolated from a smoked fish processing facility included both phage susceptible and resistant isolates. Food Microbiol. 35(1):38-48
72. Whiting RC. 1993. Modeling bacterial survival in unfavourable environments. J. Ind. Microbiol. 12:240-46
73. Zwietering MH. 2009. Quantitative risk assessment: Is more complex always better? Simple is not stupid and complex is not always more correct. Int. J. Food Microbiol. 134(1-2):57-62