Population heterogeneity of Lactobacillus plantarum WCFS1 microcolonies in response to and recovery from acid stress

Applied and Environmental Microbiology

Volumn 74, Issue 24, 2008, Pages 7750-7758

  Ingham, Colin J ^a,b   Beerthuyzen, Marke ^a,c   Vlieg, Johan Van Hylckama ^a,c  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c NIZO FOOD RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDS; CELL MEMBRANES; CYTOLOGY; GROWTH (MATERIALS); MAGNETIC RESONANCE SPECTROSCOPY; RECONNAISSANCE AIRCRAFT;

ACID STRESSES; AND RECOVERIES; CELLS LACKING; FILAMENTOUS CELLS; GELRITE; GROWTH MEDIUMS; LACTOBACILLUS PLANTARUM; LIPOPHILIC DYES; LIQUID CULTURES; MICROBIAL POPULATIONS; MICROCOLONIES; POPULATION HETEROGENEITIES; POROUS CERAMICS;

CELL CULTURE;

ENVIRONMENTAL STRESS; GROWTH RESPONSE; HETEROGENEITY; INOCULATION; MICROBIAL COMMUNITY; PH; PHENOTYPE; POPULATION STRUCTURE; SCANNING ELECTRON MICROSCOPY; SUBPOPULATION; SURVIVAL;

ARTICLE; BACTERIAL GROWTH; BACTERIUM COLONY; BACTERIUM CULTURE; CULTURE MEDIUM; ENVIRONMENTAL STRESS; LACTOBACILLUS PLANTARUM; NONHUMAN; PHENOTYPE;

ACIDS; ANTI-BACTERIAL AGENTS; CELL MEMBRANE; LACTOBACILLUS PLANTARUM; MICROSCOPY, ELECTRON, SCANNING; STRESS, PHYSIOLOGICAL;

LACTOBACILLUS PLANTARUM; POSIBACTERIA;

EID: 57449097178     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00982-08     Document Type: Article

References (43)

1. Aires, K. A., A. M. Cianciarullo, S. M. Carneiro, L. L. Villa, E. Boccardo, G. Perez-Martinez, I. Perez-Arellano, M. L. S. Oliveira, and P. L. Ho. 2006. Production of human papillomavirus type 16 L1 virus-like particles by recombinant Lactobacillus casei cells. Appl. Environ. Microbiol. 72:745-752.
2. Avery, S. V. 2006. Microbial cell individuality and the underlying sources of heterogeneity. Nat. Rev. Microbiol. 4:577-587.
3. Azcarate-Peril, M. A., O. McAuliffe, E. Altermann, S. Lick, W. M. Russell, and T. R. Klaenhammer. 2005. Microarray analysis of a two-component regulatory system involved in acid resistance and proteolytic activity in Lactobacillus acidophilus. Appl. Environ. Microbiol. 71:5794-5804.
4. Balaban, N. Q., J. Merrin, J. Chait, L. Kowalik, and S. Leibler. 2004. Bacterial persistence as a phenotypic switch. Science 305:1622- 1628.
5. Bigger, W. B. 1944. Treatment of staphylococcal infections with penicillin. Lancet 244:497-500.
6. Booth, I. R. 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.
7. Browne, N., and B. C. A. Dowds. 2002. Acid stress in the food pathogen Bacillus cereus. J. Appl. Microbiol. 92:404-414.
8. Cotter, P. D., and C. Hill. 2003. Surviving the acid test: response of grampositive bacteria to low pH. Microbiol. Mol. Biol. Rev. 67:429-453.
9. De Angelis, M., and M. Gobbetti. 2004. Environmental stress responses in Lactobacillus: a review. Proteomics 4:106-122.
10. den Besten, H. M. W., C. J. Ingham, J. E. T. van Hylckama Vlieg, M. Beerthuyzen, M. H. Zwietering, and T. Abee. 2007. Quantitative analysis of population heterogeneity of the adaptive salt stress response and outgrowth of Bacillus cereus ATCC 14579. Appl. Environ. Microbiol. 73:4797-4804.
11. Dhar, N., and J. D. McKinney. 2007. Microbial phenotypic heterogeneity and antibiotic tolerance. Curr. Opin. Microbiol. 10:30-38.
12. Elfwing, A., Y. LeMarc, J. Baranyi, and A. Ballagi. 2004. Observing growth and division of large numbers of individual bacteria by image analysis. Appl. Environ. Microbiol. 70:675-678.
13. Francois, K., F. Devlieghere, K. Smet, A. R. Standaert, A. H. Geeraerd, J. F. Van Impe, and J. Debevere. 2005. Modelling the individual cell lag phase: effect of temperature and pH on the individual cell lag distribution of Listeria monocytogenes. Int. J. Food Microbiol. 100:41-53.
14. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. SOS responses and DNA damage tolerance in prokaryotes, p. 407-464. In E. C. Friedberg, G. C. Walker, and W. Siede (ed.), DNA repair and mutagenesis. ASM Press, Washington, DC.
15. Fuentes, S., M. Egert, M. Jimenez-Valera, M. Monteoliva-Sanchez, A. Ruiz-Bravo, and H. Smidt. 2008. A strain of Lactobacillus plantarum affects segmented filamentous bacteria in the intestine of immunosuppressed mice. FEMS Microbiol. Ecol. 63:65-72.
16. Guillier, L., P. Pardon, and J. C. Augustin. 2005. Influence of stress on individual lag time distributions of Listeria monocytogenes. Appl. Environ. Microbiol. 71:2940-2948.
17. Hansen, S., K. Lewis, and M. Vulic. 2008. The role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob. Agents Chemother. 52:2718-27226.
18. Haugland, P. 1999. Handbook of fluorescent probes and research chemicals, 7th ed. Molecular Probes, Eugene, OR.
19. Hazeleger, W. C., M. Dalvoorde, and R. R. Beumer. 2006. Fluorescence microscopy of NaCl-stressed, elongated Salmonella and Listeria cells reveals the presence of septa in filaments. Int. J. Food Microbiol. 112:288-290.
20. Ingham, C. J., M. van den Ende, P. C. Wever, and P. M. Schneeberger. 2006. Rapid antibiotic sensitivity testing and trimethoprim-mediated filamentation of clinical isolates of the Enterobacteriaceae assayed on a novel porous culture support. J. Med. Microbiol. 55:1511-1519.
21. Ingham, C. J., A. Sprenkels, J. Bomer, D. Molenaar, A. van den Berg, J. E. T. van Hylckama Vlieg, and W. M. de Vos. 2007. The micro-Petri dish: a million-well growth chip for the culture and high-throughput screening of microorganisms. Proc. Natl. Acad. Sci. USA 46:18217-18222.
22. Jansson, P. E., B. Lindberg, and P. A. Sandford. 1983. Structural studies of gellan gum an extracellular polysaccharide elaborated by Pseudomonas elodea. Carbohydr. Res. 124:135-139.
23. Kelly, C. D., and O. Rahn. 1932. The growth rate of individual bacterial cells. J. Bacteriol. 23:147-153.
24. Kleerebezem, M. J. Boekhorst, R. van Kranenburg, D. Molenaar, O. P. Kuipers, R. Leer, R. Tarchini, S. A. Peters, H. M. Sandbrink, M. W. Fiers, W. Stiekema, R. M. Lankhorst, P. A. Bron, S. M. Hoffer, M. N. Groot, R. Kerkhoven, M. de Vries, B. Ursing, W. M. de Vos, and R. J. Siezen. 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. USA 100:1990-1995.
25. Klein-Marcuschamer, D., and G. Stephanopoulos. 2008. Assessing the potential of mutational strategies to elicit new phentypes in industrial strains. Proc. Natl. Acad. Sci. USA 105:2319-2324.
26. Kutalik, Z., M. Razaz, A. Elfwing, A. Ballagi, and J. Baranyi. 2005. Stochastic modelling of individual cell growth using flow chamber microscopy images. Int. J. Food Microbiol. 105:177-190.
27. Lee, K., H. G., K. Pi, and Y. J. Choi. 2008. The effect of low pH on protein expression by the probiotic bacterium Lactobacillus reuiteri. Proteomics 8:1624-1630.
28. Li, Y., J. A. Odumeru, M. Griffiths, and R. C. McKellar. 2006. Effect of environmental stresses on the mean and distribution of individual cell lag times of Escherichia coli O157:H7. Int. J. Food Microbiol. 110:278-285.
29. Li, Y., and Y. Zhang. 2007. PhoU is a persistence switch involved in persister formation and tolerance to multiple antibiotics and stresses in Escherichia coli. Antimicrob. Agents Chemother. 51:2092-2099.
30. Lin, C. C., and L. R. Casida. 1984. Gelrite as a gelling agent in media for the growth of thermophilic microorganisms. Appl. Environ. Microbiol. 47:427-429.
31. Marco, M. L., R. S. Bongers, W. M. de Vos, and M. Kleerebezem. 2007. Spatial and temporal expression of Lactobacillus plantarum genes in the gastrointestinal tracts of mice. Appl. Environ. Microbiol. 73:124-132.
32. Mattick, K. M., F. Jørgensen, J. D. Legan, M. B. Cole, J. Porter, H. M. Lappin-Scott, and T. J. Humphrey. 2000. Survival and filamentation of Salmonella enterica serovar Enteritidis PT4 and Salmonella enterica serovar Typhimurium DT104 at low water activity. Appl. Environ. Microbiol. 66:1274-1279.
33. McDonald, L. C., H. P. Fleming, and H. M. Hassan. 1990. Acid tolerance of Leuconostoc mesenteroides and Lactobacillus plantarum. Appl. Environ. Microbiol. 56:2120-2124.
34. McKellar, R. C., and A. Hawke. 2006. Assessment of distributions for fitting lag times of individual cells in bacterial populations. Int. J. Food Microbiol. 106:169-175.
35. Mellefont, L. A., T. A. McMeekin, and T. Ross. 2005. Viable count estimates of lag time responses for Salmonella typhimurium M48 subjected to abrupt osmotic shifts. Int. J. Food Microbiol. 105:399-410.
36. Neidhardt, F. C., J. L. Ingraham, and M. Schaechter. 1990. The cell cycle, p. 389-417. In F. C. Neidhardt, J. L. Ingraham, and M. Schaechter (ed.), Physiology of the bacterial cell. M. Sinauer Associates, Sunderland, MA.
37. Niven, G. W., T. Fuks, J. S. Morton, S. A. C. G. Rua, and B. M. Mackey. 2006. A novel method for measuring lag times in division of individual bacterial cells using image analysis. J. Microbiol. Methods 65:311-317.
38. Palumbo, E., C. F. Favier, M. Deghorain, P. S. Cocconcelli, C. Grangette, A. Mercenier, E. E. Vaughan, and P. Hols. 2004. Knockout of the alanine racemase gene in Lactobacillus plantarum results in septation defects and cell wall perforation. FEMS Microbiol. Lett. 233:131-138.
39. Pieterse, B., R. J. Leer, F. H. J. Schuren, and M. T. J. van der Werf. 2005. Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151:3881-3894.
40. Pogliano, J., N. Osborne, M. D. Sharp, A. Abanes-De Mello, A. Perez, Y.-L. Sun, and K. Pogliano. 1999. A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Mol. Microbiol. 31:1149-1159.
41. Ramiah, K., C. A. van Reenen, and L. M. T. Dicks. 2008. Surface-bound proteins of Lactobacillus plantarum 423 that contribute to adhesion of Caco-2 cells and their role in competitive exclusion and displacement of Clostridium sporogenes and Enterococcus faecalis. Res. Microbiol. 159:470-475.
42. Shabala, L., T. McMeekin, B. B. Bjørn Budde, and H. Siegumfeldt. 2006. Listeria innocua and Lactobacillus delbrueckii subsp. bularicus employ different strategies to cope with acid stress. Int. J. Food Microbiol. 110:1-7.
43. van de Guchte, M., P. Serror, C. Chervaux, T. Smokvina, S. D. Ehrlich, and E. Maguin. 2002. Stress responses in lactic acid bacteria. Antonie van Leeuwenhoek 82:187-216.