Promoter activity dynamics in the lag phase of Escherichia coli

BMC Systems Biology

Volumn 7, Issue , 2013, Pages

  Madar, Daniel ^a   Dekel, Erez ^a   Bren, Anat ^a   Zimmer, Anat ^a   Porat, Ziv ^a   Alon, Uri ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Bang bang control; E. coli; Lag phase; Optimal control theory; Pontryagin maximum principle; Resource allocation; Stringent response; Transcriptional program

Indexed keywords

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

FLUORESCENT DYE;

ARTICLE; BIOMASS; CELL PROLIFERATION; CYTOLOGY; ENZYMOLOGY; ESCHERICHIA COLI; FLOW CYTOMETRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; PROMOTER REGION; TIME;

BIOMASS; CELL PROLIFERATION; ESCHERICHIA COLI; FLOW CYTOMETRY; FLUORESCENT DYES; PROMOTER REGIONS, GENETIC; TIME FACTORS;

EID: 84891352625     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-7-136     Document Type: Article

References (76)

1. Müller M. Ueber den Einfluss von Fieber temperaturen auf die Wachstumsgeschwindigkeit und die Virulenz des Typhus Bacillus. Z Hyg Infektionskr 1895, 20:245.
2. Penfold WJ. On the nature of bacterial lag. J Hyg (Lond) 1914, 14:215-241. 2206768, 20474577.
3. Monod J. The growth of bacterial cultures. Annu Rev Microbiol 1949, 3:371-394.
4. Swinnen IAM, Bernaerts K, Dens EJJ, Geeraerd AH, Van Impe JF. Predictive modelling of the microbial lag phase: a review. Int J Food Microbiol 2004, 94:137-159. 10.1016/j.ijfoodmicro.2004.01.006, 15193801.
5. Koyuncu S, Andersson MG, Häggblom P. Accuracy and sensitivity of commercial PCR-based methods for detection of salmonella enterica in feed. Appl Environ Microbiol 2010, 76:2815-2822. 10.1128/AEM.02714-09, 2863422, 20228106.
6. Van Impe J, McMeekin T, Olley J, Ratkowsky D. 3rd international conference on predictive modeling in foods. Int J Food Microbiol 2002, 73:107-454.
7. Bättig P, Hathaway LJ, Hofer S, Mühlemann K. Serotype-specific invasiveness and colonization prevalence in Streptococcus pneumoniae correlate with the lag phase during in vitro growth. Microbes Infect 2006, 8:2612-2617. 10.1016/j.micinf.2006.07.013, 16938479.
8. Hathaway LJ, Brugger SD, Morand B, Bangert M, Rotzetter JU, Hauser C, Graber WA, Gore S, Kadioglu A, Mühlemann K. Capsule type of Streptococcus pneumoniae determines growth phenotype. PLoS Pathog 2012, 8:e1002574. 10.1371/journal.ppat.1002574, 3297593, 22412375.
9. Frimodt-Møller N, Sebbesen O, Frølund Thomsen V. The pneumococcus and the mouse protection test: importance of the lag phase in vivo. Chemotherapy 1983, 29:128-134. 10.1159/000238186, 6839864.
10. Baranyi J, George SM, Kutalik Z. Parameter estimation for the distribution of single cell lag times. J Theor Biol 2009, 259:24-30. 10.1016/j.jtbi.2009.03.023, 19328813.
11. Buchanan RL, Cygnarowicz ML. A mathematical approach toward defining and calculating the duration of the lag phase. Food Microbiol 1990, 7:237-240.
12. Buchanan RL, Solberg M. Interaction of sodium nitrate, oxygen and ph on growth of staphylococcus aureus. J Food Sci 1972, 37:81-85.
13. McKellar RC, Knight K. A combined discrete-continuous model describing the lag phase of Listeria monocytogenes. Int J Food Microbiol 2000, 54:171-180. 10.1016/S0168-1605(99)00204-4, 10777067.
14. Pirt SJ. Principles of microbe and cell cultivation 1975, New York: Wiley.
15. Zhou K, George SM, Métris A, Li PL, Baranyi J. Lag phase of salmonella enterica under osmotic stress conditions. Appl Environ Microbiol 2011, 77:1758-1762. 10.1128/AEM.02629-10, 3067304, 21193660.
16. Zwietering MH, Rombouts FM, van 't Riet K. Comparison of definitions of the lag phase and the exponential phase in bacterial growth. J Appl Bacteriol 1992, 72:139-145. 10.1111/j.1365-2672.1992.tb01815.x, 1556037.
17. Baranyi J, Roberts TA, McClure P. A non-autonomous differential equation to modelbacterial growth. Food Microbiol 1993, 10:43-59.
18. Srivastava AK, Volesky B. Characterization of transient cultures of clostridium acetobutylicum. Biotechnol Prog 1990, 6:408-420.
19. Baranyi J, Roberts TA. A dynamic approach to predicting bacterial growth in food. Int J Food Microbiol 1994, 23:277-294. 10.1016/0168-1605(94)90157-0, 7873331.
20. Pin C, Baranyi J. Kinetics of single cells: observation and modeling of a stochastic process. Appl Environ Microbiol 2006, 72:2163-2169. 10.1128/AEM.72.3.2163-2169.2006, 1393193, 16517667.
21. Métris A, Le Marc Y, Elfwing A, Ballagi A, Baranyi J. Modelling the variability of lag times and the first generation times of single cells of E. coli. Int J Food Microbiol 2005, 100:13-19. 10.1016/j.ijfoodmicro.2004.10.004, 15854688.
22. Elowitz MB, Levine AJ, Siggia ED, Swain PS. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186. 10.1126/science.1070919, 12183631.
23. Locke JCW, Young JW, Fontes M, Jiménez MJH, Elowitz MB. Stochastic pulse regulation in bacterial stress response. Science 2011, 334:366-369. 10.1126/science.1208144, 21979936.
24. Kaern M, Elston TC, Blake WJ, Collins JJ. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 2005, 6:451-464. 10.1038/nrg1615, 15883588.
25. Golding I, Paulsson J, Zawilski SM, Cox EC. Real-time kinetics of gene activity in individual bacteria. Cell 2005, 123:1025-1036. 10.1016/j.cell.2005.09.031, 16360033.
26. Elfwing A, LeMarc Y, Baranyi J, Ballagi A. Observing growth and division of large numbers of individual bacteria by image analysis. Appl Environ Microbiol 2004, 70:675-678. 10.1128/AEM.70.2.675-678.2004, 348858, 14766541.
27. Larsen N, Boye M, Siegumfeldt H, Jakobsen M. Differential expression of proteins and genes in the Lag phase of lactococcus lactis subsp. Lactis grown in synthetic medium and reconstituted skim milk. Appl Environ Microbiol 2006, 72:1173-1179. 10.1128/AEM.72.2.1173-1179.2006, 1392913, 16461664.
28. Cuny C, Lesbats M, Dukan S. Induction of a global stress response during the first step of Escherichia coli plate growth. Appl Environ Microbiol 2007, 73:885-889. 10.1128/AEM.01874-06, 1800750, 17142356.
29. Novotna J, Vohradsky J, Berndt P, Gramajo H, Langen H, Li X-M, Minas W, Orsaria L, Roeder D, Thompson CJ. Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol Microbiol 2003, 48:1289-1303. 10.1046/j.1365-2958.2003.03529.x, 12787356.
30. Osuna R, Lienau D, Hughes KT, Johnson RC. Sequence, regulation, and functions of fis in salmonella typhimurium. J Bacteriol 1995, 177:2021-2032. 176845, 7536730.
31. McKellar RC. Correlation between the change in the kinetics of the ribosomal RNA rrnB P2 promoter and the transition from lag to exponential phase with pseudomonas fluorescens. Int J Food Microbiol 2008, 121:11-17. 10.1016/j.ijfoodmicro.2007.10.003, 18036694.
32. McKellar RC. Effect of starvation on expression of the ribosomal RNA rrnB P2 promoter during the lag phase of pseudomonas fluorescens. Int J Food Microbiol 2007, 114:307-315. 10.1016/j.ijfoodmicro.2006.09.022, 17169452.
33. McKellar RC. Effect of sub-lethal heating and growth temperature on expression of the ribosomal RNA rrnB P2 promoter during the lag phase of pseudomonas fluorescens. Int J Food Microbiol 2007, 116:248-259. 10.1016/j.ijfoodmicro.2007.01.009, 17368596.
34. Rolfe MD, Rice CJ, Lucchini S, Pin C, Thompson A, Cameron ADS, Alston M, Stringer MF, Betts RP, Baranyi J, Peck MW, Hinton JCD. Lag phase is a distinct growth phase that prepares bacteria for exponential growth and involves transient metal accumulation. J Bacteriol 2012, 194:686-701. 10.1128/JB.06112-11, 3264077, 22139505.
35. Zaslaver A, Bren A, Ronen M, Itzkovitz S, Kikoin I, Shavit S, Liebermeister W, Surette MG, Alon U. A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Methods 2006, 3:623-628. 10.1038/nmeth895, 16862137.
36. Kaplan S, Bren A, Zaslaver A, Dekel E, Alon U. Diverse two-dimensional input functions control bacterial sugar genes. Mol Cell 2008, 29:786-792. 10.1016/j.molcel.2008.01.021, 2366073, 18374652.
37. Madar D, Dekel E, Bren A, Alon U. Negative auto-regulation increases the input dynamic-range of the arabinose system of Escherichia coli. BMC Syst Biol 2011, 5:111. 10.1186/1752-0509-5-111, 3163201, 21749723.
38. Hudson JA, Mott SJ. Comparison of lag times obtained from optical density and viable count data for a strain of pseudomonas fragi. J Food Saf 1994, 14:329-339.
39. Robinson TP, Ocio MJ, Kaloti A, Mackey BM. The effect of the growth environment on the lag phase of Listeria monocytogenes. Int J Food Microbiol 1998, 44:83-92. 10.1016/S0168-1605(98)00120-2, 9849786.
40. Kell DB, Young M. Bacterial dormancy and culturability: the role of autocrine growth factors. Curr Opin Microbiol 2000, 3:238-243. 10.1016/S1369-5274(00)00082-5, 10851153.
41. Weichart DH, Kell DB. Characterization of an autostimulatory substance produced by Escherichia coli. Microbiology 2001, 147:1875-1885.
42. Mukamolova GV, Kaprelyants AS, Young DI, Young M, Kell DB. A bacterial cytokine. Proc Natl Acad Sci U S A 1998, 95:8916-8921. 10.1073/pnas.95.15.8916, 21177, 9671779.
43. Kempner ES, Hanson FE. Aspects of light production by photobacterium fischeri. J Bacteriol 1968, 95:975-979. 252118, 5643069.
44. Turovskiy Y, Kashtanov D, Paskhover B, Chikindas ML. Quorum sensing: fact, fiction, and everything in between. Adv Appl Microbiol 2007, 62:191-234. 2391307, 17869606.
45. Pontryàgin LS, Boltyanskii VG, Gamkrelidze RV, Mishchenko EF. The mathematical theory of optimal processes 1962, New York: John Wiley.
46. Alexander RM. Optima for animals 1996, Princeton: Princeton University Press.
47. Cai L, Friedman N, Xie XS. Stochastic protein expression in individual cells at the single molecule level. Nature 2006, 440:358-362. 10.1038/nature04599, 16541077.
48. Levin-Reisman I, Gefen O, Fridman O, Ronin I, Shwa D, Sheftel H, Balaban NQ. Automated imaging with ScanLag reveals previously undetectable bacterial growth phenotypes. Nat Methods 2010, 7:737-739. 10.1038/nmeth.1485, 20676109.
49. Ishay J, Bytinski-Saltz H, Shulov A. Contributions to the bionomics of the oriental hornet Vespa orientalis. Isr J Entomol 1967, 2:45-106.
50. Macevicz S, Oster G. Modeling social insect populations II: optimal reproductive strategies in annual eusocial insect colonies. Behav Ecol Sociobiol 1976, 1:265-282.
51. Oster GF, Wilson EO. Caste and ecology in the social insects. (Mpb-12) 1979, Princeton: Princeton University Press.
52. Shoval O, Sheftel H, Shinar G, Hart Y, Ramote O, Mayo A, Dekel E, Kavanagh K, Alon U. Evolutionary trade-offs, pareto optimality, and the geometry of phenotype space. Science 2012, 336:1157-1160. 10.1126/science.1217405, 22539553.
53. Cashel M, Kalbacher B. The control of ribonucleic acid synthesis in Escherichia coli. V. Characterization of a nucleotide associated with the stringent response. J Biol Chem 1970, 245:2309-2318.
54. Cashel M, Gentry DR, Hernandez VH, Vinella D. The stringent response. Escherichia coli & salmonella typhimurium: cellular & molecular biology. Volume 1 1996, 1458-1496. Washington DC: ASM Press, Ingraham JL, Neidhardt FC, Ingraham JL, Neidhardt FC, 2.
55. Schneider DA, Ross W, Gourse RL. Control of rRNA expression in Escherichia coli. Curr Opin Microbiol 2003, 6:151-156. 10.1016/S1369-5274(03)00038-9, 12732305.
56. Bouveret E, Battesti A. The stringent response. In Bacterial stress response. 2nd Edition. Edited by Storz G, Hengge R 2011, Washington, DC: ASM Press.
57. Yamamotoya T, Dose H, Tian Z, Fauré A, Toya Y, Honma M, Igarashi K, Nakahigashi K, Soga T, Mori H, Matsuno H. Glycogen is the primary source of glucose during the lag phase of E. coli proliferation. Biochim Biophys Acta 1824, 2012:1442-1448.
58. Zhou K, George SM, Li PL, Baranyi J. Effect of periodic fluctuation in the osmotic environment on the adaptation of Salmonella. Food Microbiol 2012, 30:298-302. 10.1016/j.fm.2011.09.016, 22265315.
59. Itzkovitz S, Blat IC, Jacks T, Clevers H, van Oudenaarden A. Optimality in the development of intestinal crypts. Cell 2012, 148:608-619. 10.1016/j.cell.2011.12.025, 3696183, 22304925.
60. Oxman E, Alon U, Dekel E. Defined order of evolutionary adaptations: experimental evidence. Evolution 2008, 62:1547-1554. 10.1111/j.1558-5646.2008.00397.x, 18410537.
61. Cormack BP, Valdivia RH, Falkow S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 1996, 173(1 Spec No):33-38.
62. Hart Y, Madar D, Yuan J, Bren A, Mayo AE, Rabinowitz JD, Alon U. Robust control of nitrogen assimilation by a bifunctional enzyme in E. Coli. Mol Cell 2011, 41:117-127.
63. Hershey AD. Factors limiting bacterial growth. J Bacteriol 1939, 37:285-299. 374464, 16560205.
64. Pin C, Baranyi J. Single-cell and population lag times as a function of cell age. Appl Environ Microbiol 2008, 74:2534-2536. 10.1128/AEM.02402-07, 2293159, 18296533.
65. D'Arrigo M, de Fernando GDG, Velasco de Diego R, Ordóñez JA, George SM, Pin C. Indirect measurement of the lag time distribution of single cells of listeria innocua in food. Appl Environ Microbiol 2006, 72:2533-2538. 10.1128/AEM.72.4.2533-2538.2006, 1449042, 16597954.
66. Biesta-Peters EG, Mols M, Reij MW, Abee T. Physiological parameters of Bacillus cereus marking the end of acid-induced lag phases. Int J Food Microbiol 2011, 148:42-47. 10.1016/j.ijfoodmicro.2011.04.024, 21592605.
67. Gennis RB, Stewart V. Respiration. Escherichia Coli & Salmonella Typhimurium: Cellular & Molecular Biology. Volume 1 217-261. Washington, DC: ASM Press, Ingraham JL, Neidhardt FC, 2.
68. Guillier L, Pardon P, Augustin J-C. Influence of stress on individual lag time distributions of listeria monocytogenes. Appl Environ Microbiol 2005, 71:2940-2948. 10.1128/AEM.71.6.2940-2948.2005, 1151854, 15932988.
69. Marie D, Vaulot D, Partensky F. Application of the novel nucleic acid dyes YOYO-1, YO-PRO-1, and PicoGreen for flow cytometric analysis of marine prokaryotes. Appl Environ Microbiol 1996, 62:1649-1655. 167939, 8633863.
70. Gasol JM, del Giorgio PA. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci Mar 2000, 64:197-224.
71. Kamiya E, Izumiyama S, Nishimura M, Mitchell JG, Kogure K. Effects of fixation and storage on flow cytometric analysis of marine bacteria. J Oceanogr 2007, 63:101-112.
72. Günther S, Hübschmann T, Rudolf M, Eschenhagen M, Röske I, Harms H, Müller S. Fixation procedures for flow cytometric analysis of environmental bacteria. J Microbiol Methods 2008, 75:127-134. 10.1016/j.mimet.2008.05.017, 18584902.
73. Monfort P, Baleux B. Comparison of flow cytometry and epifluorescence microscopy for counting bacteria in aquatic ecosystems. Cytometry 1992, 13:188-192. 10.1002/cyto.990130213, 1547667.
74. George TC, Fanning SL, Fitzgerald-Bocarsly P, Fitzgeral-Bocarsly P, Medeiros RB, Highfill S, Shimizu Y, Hall BE, Frost K, Basiji D, Ortyn WE, Morrissey PJ, Lynch DH. Quantitative measurement of nuclear translocation events using similarity analysis of multispectral cellular images obtained in flow. J Immunol Methods 2006, 311:117-129. 10.1016/j.jim.2006.01.018, 16563425.
75. Rajwa B, Venkatapathi M, Ragheb K, Banada PP, Hirleman ED, Lary T, Robinson JP. Automated classification of bacterial particles in flow by multiangle scatter measurement and support vector machine classifier. Cytometry Part A 2008, 73A:369-379.
76. Yamaguchi N, Torii M, Uebayashi Y, Nasu M. Rapid, Semiautomated Quantification of Bacterial Cells in Freshwater by Using a Microfluidic Device for On-Chip Staining and Counting. Appl Environ Microbiol 2011, 77:1536-1539. 10.1128/AEM.01765-10, 3067242, 21169431.