Induction of viable but non-culturable (VBNC) state in Salmonella cultured in M9 minimal medium containing high glucose

Biological and Pharmaceutical Bulletin

Volumn 37, Issue 10, 2014, Pages 1617-1625

  Morishige, Yuta ^a   Tanda, Masaaki ^a   Fujimori, Ko ^a   Mino, Yoshiki ^a   Amano, Fumio ^a  

^a OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

Formate; Glucose; Prolonged culture; Salmonella; Viable but non culturable (VBNC) induction

Indexed keywords

FORMIC ACID; GLUCOSE; CULTURE MEDIUM;

ARTICLE; BACTERIAL CELL; BACTERIUM CULTURE; CELL DEATH; CELL DENSITY; CELL DIVISION; CELL GROWTH; CELL RESPIRATION; CELL SURVIVAL; CELL VIABILITY; COLONY FORMING UNIT; CULTURE MEDIUM; CYTOTOXICITY; GLUCOSE METABOLISM; GROWTH RATE; M9 MINIMAL MEDIUM; NONHUMAN; PH; SALMONELLA ENTERITIDIS; BACTERIAL COUNT; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MICROBIAL VIABILITY; PHARMACOLOGY; PROCEDURES; SALMONELLA;

COLONY COUNT, MICROBIAL; CULTURE MEDIA; GLUCOSE; MICROBIAL VIABILITY; SALMONELLA;

EID: 84908020533     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b14-00322     Document Type: Article

References (42)

1. Braden C-R. Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clinical Infectious Diseases, 43, 512-517 (2006).
2. Multistate outbreaks of Salmonella infections associated with live poultry-United States, 2007. JAMA, 301, 818-820 (2009).
3. Hiramatsu R, Matsumoto M, Sakae K, Miyazaki Y. Ability of Shiga toxin-producing Escherichia coli and Salmonella spp. to survive in a desiccation model system and in dry foods. Appl. Environ. Microbiol., 71, 6657-6663 (2005).
4. Little CL, Rhoades JR, Hucklesby L, Greenwood M, Surman-Lee S, Bolton FJ, Meldrum R, Wilson I, McDonald C, de Pinna E, Threlfall EJ, Chan CH. Survey of Salmonella contamination of raw shell eggs used in food service premises in the United Kingdom, 2005 through 2006. J. Food Prot., 71, 19-26 (2008).
5. Pedersen TB, Olsen JE, Bisgaard M. Persistence of Salmonella Senftenberg in poultry production environments and investigation of its resistance to desiccation. Avian Pathol., 37, 421-427 (2008).
6. Infectious Disease Surveillance Center. Salmonella, food poisoning, outbreak, S. Enteritidis, S. Typhimurium, S. Infantis, phage typing, egg, chicken meat, reptile. IASR: Infectious Agents Surveillance Report, 30-8 Salmonellosis, National Institute of Infectious Diseases, Tokyo (2009).
7. Wei S-H, Huang AS, Liao Y-S, Liu Y-L, Chiou C-S. A large outbreak of salmonellosis associated with sandwiches contaminated with multiple bacterial pathogens purchased via an online shopping service. Foodborne Pathog. Dis., 11, 230-233 (2014).
8. Jackson BR, Griffin PM, Cole D, Walsh KA, Chai S. Outbreakassociated Salmonella enterica serotypes and food commodities, United States, 1998-2008, J. Emerg. Infect. Dis., 19, 1239-1244 (2013).
9. Liu Y-L, Schmid D, Voss AS, Kasper S, Lassnig H, Ableitner O, Kornschober C, Karnthaler U, Allerberger FA. 2010 Austrian Salmonella Enteritidis PT4 outbreak associated with a laying hen holding previously involved in an S. Enteritidis PT4 cluster: pitfalls of regulatory responses in risk management. J. Infect. Public Health, 5, 332-339 (2012).
10. Zenner D, Janmohamed K, Lane C, Little C, Charlett A, Adak GK, Morgan D. The serotype case-case design: a direct comparison of a novel methodology with a case-control study in a national Salmonella Enteritidis PT14b outbreak in England and Wales. Epidemiol. Infect., 141, 2346-2353 (2013).
11. Amano F. SEp22, Salmonella Dps, a key molecule bearing both pathogenicity and resistance to environmental stresses. J. Health Sci., 57, 458-471 (2011).
12. Terai S, Yamasaki M, Igimi S, Amano F. Expression and degradation of SEp22, a pathogenicity-related protein of Salmonella Dps, in Salmonella enterica serovar Enteritidis isolated from the poultry farms in Japan. Biosci. Microflora, 24, 113-118 (2 0 0 5).
13. Miller JH. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y. (1972).
14. Terai S, Yasuda M, Amano F. Regulation of SEp22 expression in Salmonella enterica ssp. enterica serovar Enteritidis by culture medium. Microbes Environ., 21, 36-43 (2006).
15. Halsey TA, Vazquez-Torres A, Gravdahl DJ, Fang FC, Libby SJ. The ferritin-like Dps protein is required for Salmonella enterica serovar Typhimurium oxidative stress resistance and virulence. Infect. Immun., 72, 11 55-115 8 (2 0 0 4).
16. Tamura A, Yamasaki M, Okutani A, Igimi S, Saitoh N, Ekawa T, Ohta H, Katayama Y, Amano F. Dry-resistance of Salmonella enterica ssp. enterica serovar Enteritidis is regulated by both SEp22, a novel pathogenicity-related factor of Salmonella, and nutrients. Microbes Environ., 24, 121-127 (2009).
17. Colwell RR, Brayton PR, Grimes DJ, Roszak DB, Huq SA, Palmer LM. Viable but non-culturable Vibrio cholerae and related pathogens in the environment: implications for release of genetically engineered microorganisms. Nature Biotechnol., 3, 817-820 (1985).
18. Oliver JD. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev., 34, 415-425 (2010).
19. Asakura H, Kawamoto K, Haishima Y, Igimi S, Yamamoto S, Makino S. Differential expression of the outer membrane protein W (OmpW) stress response in enterohemorrhagic Escherichia coli O157:H7 corresponds to the viable but non-culturable state. Res. Microbiol., 159, 709-717 (2008).
20. Cook KL, Bolster CH. Survival of Campylobacter jejuni and Escherichia coli in groundwater during prolonged starvation at low temperatures. J. Appl. Microbiol., 103, 573-583 (2007).
21. 2-degrading compounds. Arch. Microbiol., 172, 63-67 (1999).
22. Wong H-C, Liu S-H. Characterization of the low-salinity stress in Vibrio vulnificus. J. Food Prot., 71, 416-419 (20 0 8).
23. Cappelier JM, Lazaro B, Rossero A, Fernandez-Astorga A, Federighi M. Double staining (CTC-DAPI) for detection and enumeration of viable but non-culturable Campylobacter jejuni cells. Vet. Res., 28, 547-555 (1997).
24. Rodriguez GG, Phipps D, Ishiguro K, Ridgway HF. Use of a fuorescent redox probe for direct visualization of actively respiring bacteria. Appl. Environ. Microbiol., 58, 1801-1808 (1992).
25. Nelson DL, Cox MM. Lehninger Principles of Biochemistry, 3rd ed., Worth Publishers, pp. 408-409 (2000).
26. Dawson R M C, Elliott WH, Jones KM. Data for Biochemical Research, 3rd ed., Oxford Science Publications, pp. 424-425 (1986).
27. Morishige Y, Fujimori K, Amano F. Differential resuscitative effect of pyruvate and its analogues on VBNC (Viable But Non-Culturable) Salmonella. Microbes Environ., 28, 180-186 (2013).
28. Varma A, Palsson BO. Stoichiometric fux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W 3 11 0. Appl. Environ. Microbiol., 60, 3724-3731 (1994).
29. Xu B, Jahic M, Blomsten G, Enfors SO. Glucose overfow metabolism and mixed-acid fermentation in aerobic large-scale fed-batch processes with Escherichia coli. Appl. Microbiol. Biotechnol., 51, 564-571 (1999).
30. Xu B, Jahic M, Enfors SO. Modeling of overfow metabolism in batch and fed-batch cultures of Escherichia coli. Biotechnol. Prog., 15, 81-90 (1999).
31. Cerca F, Andrade F, França Â, Andrade EB, Ribeiro A, Almeida AA, Cerca N, Pier G, Azeredo J, Vilanova M. Staphylococcus epidermidis biofilms with higher proportions of dormant bacteria induce a lower activation of murine macrophages. J. Med. Microbiol., 60, 1717-1724 (2011).
32. Sawers G, Böck A. Anaerobic regulation of pyruvate formate-lyase from Escherichia coli K-12. J. Bacteriol., 170, 5330-5336 (1988).
33. Sawers G, Watson G. A glycyl radical solution: oxygen-dependent interconversion of pyruvate formate-lyase. Mol. Microbiol., 29, 945-954 (1998).
34. Du L, Su Y, Sun D, Zhu W, Wang J, Zhuang X, Zhou S, Lu Y. Formic acid induces Yca1p-independent apoptosis-like cell death in the yeast Saccharomyces cerevisiae. FEMS Yeast Res., 8, 531-539 (2008).
35. Richter C, Gogvadze V, Laffranchi R, Schlapbach R, Schweizer M, Suter M, Walter P, Yaffee M. Oxidants in mitochondria: from physiology to diseases. Biochim. Biophys. Acta, 1271, 67-74 (1995).
36. Wolfe AJ. The acetate switch. Microbiol. Mol. Biol. Rev., 69, 12-50 (2005).
37. Enfors S-O, Jahic M, Rozkov A, Xu B, Hecker M, Jürgen B, Krüger E, Schweder T, Hamer G, O'Beirne D, Noisommit-Rizzi N, Reuss M, Boone L, Hewitt C, McFarlane C, Nienow A, Kovacs T, Trägårdh C, Fuchs L, Revstedt J, Friberg PC, Hjertager B, Blomsten G, Skogman H, Hjort S, Hoeks F, Lin H-Y, Neubauer P, van der Lans R, Luyben K, Vrabel P, Manelius Å. Physiological responses to mixing in large scale bioreactors. J. Biotechnol., 85, 175-185 (20 01).
38. Lara AR, Vazquez-Limón C, Gosset G, Bolívar F, López-Munguía A, Ramírez OT. Engineering Escherichia coli to improve culture performance and reduce formation of by-products during recombinant protein production under transient intermittent anaerobic conditions. Biotechnol. Bioeng., 94, 116 4-1175 (2 0 0 6).
39. Nikel PI, de Almeida A, Giordano AM, Pettinari MJ. Redox driven metabolic tuning: carbon source and aeration affect synthesis of poly (3-hydroxybutyrate) in Escherichia coli. Bioeng. Bugs, 1, 291-295 (2010).
40. Wagner A, Schultz S, Bomke J, Pils T, Lehmann W, Knappe J. YfiD of Escherichia coli and Y06I of bacteriophage T4 as autonomous glycyl radical cofactors reconstituting the catalytic center of oxygen-fragmented pyruvate formate-lyase. Biochem. Biophys. Res. Commun., 285, 456-462 (2001).
41. Ojima Y, Suryadarma P, Tsuchida K, Taya M. Accumulation of pyruvate by changing the redox status in Escherichia coli. Biotechnol. Lett., 34, 889-893 (2012).
42. O'Donnell-Tormey J, Nathan CF, Lanks K, De Boer CJ, de la Harpe J. Secretion of pyruvate. An antioxidant defense of mammalian cells. J. Exp. Med., 165, 500-514 (1987).