Predictive microbiology theory and application: Is it all about rates?

Food Control

Volumn 29, Issue 2, 2013, Pages 290-299

  McMeekin, Tom ^a   Olley, June ^a   Ratkowsky, David ^a   Corkrey, Ross ^a   Ross, Tom ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

Author keywords

"Source sink"; Antibiotic resistance; Biocide resistance; Bioinformatics; Biological rates; Growth rate temperature response; Mechanistic model; Persister cells; Predictive microbiology; Protein folding thermodynamics; Stringent response; Systems biology

Indexed keywords

EID: 84867018448     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2012.06.001     Document Type: Article

References (137)

1. Adams M.R., Little C.L., Easter M.C. Modeling the effect of pH, acidulant and temperature on the growth rate of Yersinia enterocolitica. Journal of Applied Bacteriology 1991, 71(1):65-71.
2. Anastasiou D., Poulogiannis G., Asara J.M., Boxer M.B., Jiang J.-k., Shen M., et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 2011, 334(6060):1278-1283.
3. Anfinsen C.B. Principles that govern folding of protein chains. Science 1973, 181(4096):223-230.
4. Aravind L., Tatusov R.L., Wolf Y.I., Walker D.R., Koonin E.V. Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends in Genetics 1998, 14(11):442-444.
5. Bajard S., Rosso L., Fardel G., Flandrois J.P. The particular behaviour of Listeria monocytogenes under sub-optimal conditions. International Journal of Food Microbiology 1996, 29(2-3):201-211.
6. Balaban N.Q., Merrin J., Chait R., Kowalik L., Leibler S. Bacterial persistence as a phenotypic switch. Science 2005, 305(5690):1622-1625.
7. Belenky P., Collins J.J. Antioxidant strategies to tolerate antibiotics. Science 2011, 334(6058):915-916.
8. Bigger J.W. Treatment of staphylococcal infections with penicillin. Lancet 1944, ii:497-500.
9. Blankenship L.C., Craven S.E., Leffler R.G., Custer C. Growth of Clostridium perfringens in cooked chili during cooling. Applied and Environmental Microbiology 1988, 54(5):1104-1108.
10. Bloomfield S.F., Stewart G.S.A.B., Dodd C.E.R., Botth I.R., Power E.G.M. Comment: the viable but non-culturable phenomenon explained?. Microbiology 1998, 144:1-2.
11. Campbell A. Synchronization of cell division. Bacteriological Reviews 1957, 21(4):263-272.
12. Caro-Quintero A., Deng J., Auchtung J., Brettar I., Hofle M.G., Klappenbach J., et al. Unprecedented levels of horizontal gene transfer among spatially co-occurring Shewanella bacteria from the Baltic Sea. ISME Journal 2011, 5(1):131-140.
13. Cashel M. Regulation of bacterial ppGpp and pppGpp. Annual Review of Microbiology 1975, 29:301-318.
14. Chattopadhyay S., Feldgarden M., Weissman S.J., Dykhuizen D.E., van Belle G., Sokurenko E.V. Haplotype diversity in "source-sink" dynamics of Escherichia coli urovirulence. Journal of Molecular Evolution 2007, 64(2):204-214.
15. Chen P.Q., Shakhnovich E.I. Thermal adaptation of viruses and bacteria. Biophysical Journal 2010, 98(7):1109-1118.
16. Chesbro W., Evans T., Eifert R. Very slow growth of Escherichia coli. Journal of Bacteriology 1979, 139(2):625-638.
17. Chesney J.A., Eaton J.W., Mahoney J.R. Bacterial glutathione: a sacrificial defense against chlorine compounds. Journal of Bacteriology 1996, 178(7):2131-2135.
18. Cooper S. The origins and meaning of the Schaechter-Maaløe-Kjeldgaard experiments. Journal of General Microbiology 1993, 139:1117-1124.
19. Corkrey R., Olley J., Ratkowsky D., McMeekin T., Ross T. Universality of thermodynamic constants governing biological growth rates. PloS One 2012, 7(2):e32003.
20. Cornet I., Van Derlinden E., Cappuyns A.M., Van Impe J.F. Heat stress adaptation of Escherichia coli under dynamic conditions: effect of inoculum size*. Letters in Applied Microbiology 2010, 51(4):450-455.
21. Cossart P. Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(49):19484-19491.
22. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284(5418):1318-1322.
23. D'Alessandro A., Zolla L. We are what we eat: food safety and proteomics. Journal of Proteome Research 2012, 11:26-36.
24. Davidson P.M., Harrison M.A. Resistance and adaptation to food antimicrobials, sanitizers, and other process controls. Food Technology 2002, 56(11):69-78.
25. Dell A.I., Pawar S., Savage V.M. Systematic variation in the temperature dependence of physiological and ecological traits. Proceedings of the National Academy of Sciences 2011, 108(26):10591-10596.
26. Dennehy J.J., Friedenberg N.A., McBride R.C., Holt R.D., Turner P.E. Experimental evidence that source genetic variation drives pathogen emergence. Proceedings of the Royal Society B-Biological Sciences 2010, 277(1697):3113-3121.
27. Dickinson B.C., Chang C.J. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nature Chemical Biology 2011, 7(8):504-511.
28. Dodd C.E.R., Sharman R., Bloomfield S.F., Booth I.R., Stewart G.S.A.B. Inimical processes: bacterial self-destruction and sub-lethal injury. Trends in Food Science & Technology 1997, 8(7):238-241.
29. EFSA.(European Food Safety Authority) Assessment of the possible effect of the four antimicrobial treatment substances on the emergence of antimicrobial resistance. The EFSA Journal 2008, 659:1-26.
30. van Elsas J.D., Chiurazza M., Mallon C.A., Elhottova D., Kristufek V., Salles J.K. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:7897-7901.
31. Fauvart M., De Grootet V.N., Michiels J. Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. Journal of Medical Microbiology 2011, 60(6):699-709.
32. Gentry D.R., Ingraham K.A., Stanhope M.J., Rittenhouse S., Jarvest R.L., O'Hanlon P.J., et al. Variable sensitivity to bacterial methionyl-tRNA synthetase inhibitors reveals subpopulations of Streptococcus pneumoniae with two distinct methionyl-tRNA synthetase genes. Antimicrobial Agents and Chemotherapy 2003, 47(6):1784-1789.
33. Ghosh K., Dill K. Cellular proteomes have broad distributions of protein stability. Biophysical Journal 2010, 99(12):3996-4002.
34. Gilbert P., Collier P.J., Brown M.R.W. Influence of growth-rate on susceptibility to antimicrobial agents - biofilms, cell-cycle, dormancy, and stringent response. Antimicrobial Agents and Chemotherapy 1990, 34(10):1865-1868.
35. Goffin P., van de Bunt B., Giovane M., Leveau J.H.J., Hoppener-Ogawa S., Teusink B., et al. Understanding the physiology of Lactobacillus plantarum at zero growth. Molecular Systems Biology 2010, 6. 10.1038/msb.2010.6.
36. Govindarajan D., Goldstein R.A. Why are some protein structures so common. Proceedings of the National Academy of Sciences, USA 1996, 93:3341-3345.
37. Griffiths M.W., Phillips J.D. Prediction of the shelf-life of pasteurized milk at different storage temperatures. Journal of Applied Bacteriology 1988, 65(4):269-278.
38. Guerra C., Morris D., Sipin A., Kung S., Franklin M., Gray D., et al. Glutathione and adaptive immune responses against Mycobacterium tuberculosis infection in healthy and HIV infected individuals. PLoS One 2011, 6(12):e28378.
39. Hamanaka R.B., Chandel N.S. Warburg effect and redox balance. Science 2011, 334(6060):1219-1220.
40. Hehemann J.H., Correc G., Barbeyron T., Helbert W., Czjzek M., Michel G. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 2010, 464(7290):908-912.
41. Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiology and Molecular Biology Reviews 2002, 66(3):373-395.
42. Hermsen R., Hwa T. Sources and sinks: a stochastic model of evolution in heterogeneous environments. Physical Review Letters 2010, 105(24):248104.
43. Huang L. Growth kinetics of Escherichia coli O157:H7 in mechanically-tenderized beef. International Journal of Food Microbiology 2010, 140(1):40-48.
44. Huang L. A new mechanistic growth model for simultaneous determination of lag phase duration and exponential growth rate and a new Bělehradék-type model for evaluating the effect of temperature on growth rate. Food Microbiology 2011, 28(4):770-776.
45. Ihssen J., Egli T. Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology-SGM 2004, 150:1637-1648.
46. Imlay J.A. A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli. Journal of Biological Chemistry 1995, 270(34):19767-19777.
47. Jameson J.F. A discussion of the dynamics of Salmonella enrichment. Journal of Hygiene (Cambridge) 1962, 60:193-207.
48. Jefferies C.J., Brain P. A mathematical model of pollen-tube penetration in apple styles. Planta 1984, 160(1):52-58.
49. Jozefczuk S., Klie S., Catchpole G., Szymanski J., Cuadros-Inostroza A., Steinhauser D., et al. Metabolomic and transcriptomic stress response of Escherichia coli. Molecular Systems Biology 2010, 6. 10.1038/msb.2010.18.
50. Kamp H.D., Higgins D.E. Transcriptional and post-transcriptional regulation of the GmaR antirepressor governs temperature-dependent control of flagellar motility in Listeria monocytogenes. Molecular Microbiology 2009, 74(2):421-435.
51. Kastbjerg V.G., Larsen M.H., Gram L., Ingmer H. Influence of sublethal concentrations of common disinfectants on expression of virulence genes in Listeria monocytogenes. Applied and Environmental Microbiology 2010, 76(1):303-309.
52. Kastbjerg V.G., Nielsen D.S., Arneborg N., Gram L. Response of Listeria monocytogenes to disinfection stress at the single-cell and population levels as monitored by intracellular pH measurements and viable-cell counts. Applied and Environmental Microbiology 2009, 75(13):4550-4556.
53. Kim J.-S., Heo P., Yang T.-J., Lee K.-S., Cho D.-H., Kim B.T., et al. Selective killing of bacterial persisters by a single chemical compound without affecting normal antibiotic-sensitive cells. Antimicrobial Agents and Chemotherapy 2011, 55(11):5380-5383.
54. Kjeldgaard N.O., Maaløe O., Schaechter M. The transition between different physiological states during balanced growth of Salmonella typhimurium. Journal of General Microbiology 1958, 19(3):607-616.
55. Knies J.L., Kingsolver J.G. Erroneous Arrhenius: modified Arrhenius model best explains the temperature dependence of ectotherm fitness. American Naturalist 2010, 176(2):227-233.
56. Kolter R. Growth in studying the cessation of growth. Journal of Bacteriology 1999, 181(3):697-699.
57. Koonin E.V., Makarova K.S., Aravind L. Horizontal gene transfer in prokaryotes: quantification and classification. Annual Review of Microbiology 2001, 55:709-742.
58. Koseki S. Microbial responses viewer (MRV): a new ComBase-derived database of microbial responses to food environments. International Journal of Food Microbiology 2009, 134(1-2):75-82.
59. Laland K.N., Sterelny K., Odling-Smee J., Hoppitt W., Uller T. Cause and effect in biology revisited: is Mayr's proximate-ultimate dichotomy still useful?. Science 2011, 334(6062):1512-1516.
60. Lange R., Hengge Aronis R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Molecular Microbiology 1991, 5(1):49-59.
61. Lange R., Hengge-Aronis R. The cellular concentration of the sigma(s) subunit of RNA-polymerase in Escherichia coli is controlled at the levels of transcription translation, and protein stability. Genes & Development 1994, 8(13):1600-1612.
62. Lauro F.M., McDougald D., Thomas T., Williams T.J., Egan S., Rice S., et al. The genomic basis of trophic strategy in marine bacteria. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(37):15527-15533.
63. Levin B.R., Rozen D.E. Opinion - non-inherited antibiotic resistance. Nature Reviews Microbiology 2006, 4(7):556-562.
64. Lewis K. Riddle of biofilm resistance. Antimicrobial Agents and Chemotherapy 2001, 45(4):999-1007.
65. Li W.K.W. Microbial uptake of radiolabeled substrates - estimates of growth-rates from time course measurements. Applied and Environmental Microbiology 1984, 47(1):184-192.
66. Li W.K.W., Dickie P.M. Temperature characteristics of photosynthetic and heterotrophic activities - seasonal variations in temperate microbial plankton. Applied and Environmental Microbiology 1987, 53(10):2282-2295.
67. Lobkovsky A.E., Wolf Y.I., Koonin E.V. Universal distribution of protein evolution rates as a consequence of protein folding physics. Proceedings of the National Academy of Sciences 2010, 107(7):2983-2988.
68. Lobry J.R., Rosso L., Flandrois J.-P. A FORTRAN subroutine for the determination of parameters confidence in non-linear models. Binary 1991, 4:86-93.
69. Lund E., Kjeldgaard N.O. Protein synthesis and formation of guanosinetetraphosphate. FEBS Letters 1972, 26(1):306.
70. McKellar R.C., Lu X.W. Modeling microbial responses in foods 2004, CRC Press, Boca Raton, USA.
71. McMeekin T., Bowman J., McQuestin O., Mellefont L., Ross T., Tamplin M. The future of predictive microbiology: strategic research, innovative applications and great expectations. International Journal of Food Microbiology 2008, 128(1):2-9.
72. McMeekin T.A., Chandler R.E., Doe P.E., Garland C.D., Olley J., Putro S., et al. Model for combined effect of temperature and salt concentration/water activity on the growth rate of Staphylococcus xylosus. Journal of Applied Bacteriology 1987, 62(6):543-550.
73. McMeekin T.A., Olley J., Ratkowsky D.A., Ross T. Predictive microbiology theory and application: is it all about rates?. Seventh International Conference on Predictive Modelling in Foods - Conference Proceedings 2011, 17-20. UCD, DIT, Teagasc, Dublin, Ireland. E. Cummins, J.M. Frias, V.P. Valdramidis (Eds.).
74. McMeekin T.A., Olley J.N., Ross T., Ratkowsky D.A. Predictive microbiology: Theory and application 1993, Research Studies Press Ltd., Taunton, UK.
75. Mallam A.L., Jackson S.E. Knot formation in newly translated proteins is spontaneous and accelerated by chaperonins. Nature Chemical Biology 2012, 8:147-153.
76. Mauder N., Williams T., Fritsch F., Kuhn M., Beier D. Response regulator DegU of Listeria monocytogenes controls temperature-responsive flagellar gene expression in its unphosphorylated state. Journal of Bacteriology 2008, 190(13):4777-4781.
77. Mayr E. Cause and effect in biology. Kinds of causes, predictability, and teleology are viewed by a practicing biologist. Science 1961, 134(348):1501.
78. Mejlholm O., Gunvig A., Borggaard C., Blom-Hanssen J., Mellefont L., Ross T., et al. Predicting growth rates and growth boundary of Listeria monocytogenes - an international validation study with focus on processed and ready-to-eat meat and seafood. International Journal of Food Microbiology 2010, 141(3):137-150.
79. Meyer B. Does microbial resistance to biocides create a hazard to food hygiene?. International Journal of Food Microbiology 2006, 112(3):275-279.
80. Monod J. Recherches sur la croissance des cultures bacterienne 1942, Herman and Cie, Paris, France.
81. Monod J. The growth of bacterial cultures. Annual Review of Microbiology 1949, 3:371-394.
82. Mueller R.S., Denef V.J., Kalnejais L.H., Suttle K.B., Thomas B.C., Wilmes P., et al. Ecological distribution and population physiology defined by proteomics in a natural microbial community. Molecular Systems Biology 2010, 6. 10.1038/msb.2010.30.
83. Mulcahy L.R., Burns J.L., Lory S., Lewis K. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. Journal of Bacteriology 2010, 192(23):6191-6199.
84. Navarro Llorens J.M., Tormo A., Martinez-Garcia E. Stationary phase in gram-negative bacteria. FEMS Microbiology Reviews 2010, 34(4):476-495.
85. Neidhardt F.C. Bacterial growth: constant obsession with dN/dt. Journal of Bacteriology 1999, 181(24):7405-7408.
86. Nguyen D., Joshi-Datar A., Lepine F., Bauerle E., Olakanmi O., Beer K., et al. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 2011, 334(6058):982-986.
87. Niemela S.I., Oivanen P. Transition from growth to death in populations of Klebsiella terrigena and other enterobacteriaceae in relation to temperature. FEMS Microbiology Letters 1992, 91(2):181-185.
88. Ohta F., Hirahara T. Rate of degradation in cool-stored carp muscle. Memoirs Faculty of Fisheries Kagoshima University 1977, 26:97-102.
89. Olley J., Ratkowsky D.A. Temperature function integration and importance in the storage and distribution of fresh food above the freezing point. Food Technology Australia 1973, 25:66-73.
90. Papp B., Notebaart R.A., Pal C. Systems-biology approaches for predicting genomic evolution. Nature Reviews Genetics 2011, 12(9):591-602.
91. Park Y.J., Chen J. Inactivation of Shiga toxin-producing Escherichia coli (STEC) and degradation and removal of cellulose from STEC surfaces by using selected enzymatic and chemical treatments. Applied and Environmental Microbiology 2011, 77(24):8532-8537.
92. Poelwijk F.J., Kiviet D.J., Weinreich D.M., Tans S.J. Empirical fitness landscapes reveal accessible evolutionary paths. Nature 2007, 445(7126):383-386.
93. Poole K. Mechanisms of bacterial biocide and antibiotic resistance. Journal of Applied Microbiology 2002, 92:55S-64S.
94. Potrykus K., Murphy H., Philippe N., Cashel M. ppGpp is the major source of growth rate control in E. coli. Environmental Microbiology 2011, 13(3):563-575.
95. Price P.B., Sowers T. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(13):4631-4636.
96. Raes J., Letunic I., Yamada T., Jensen L.J., Bork P. Toward molecular trait-based ecology through integration of biogeochemical, geographical and metagenomic data. Molecular Systems Biology 2011, 7:374. 10.1038/msb.2011.6.
97. Ratkowsky D.A., Lowry R.K., McMeekin T.A., Stokes A.N., Chandler R.E. Model for bacterial culture growth rate throughout the entire biokinetic temperature-range. Journal of Bacteriology 1983, 154(3):1222-1226.
98. Ratkowsky D.A., Olley J., McMeekin T.A., Ball A. Relationship between temperature and growth-rate of bacterial cultures. Journal of Bacteriology 1982, 149(1):1-5.
99. Ratkowsky D.A., Olley J., Ross T. Unifying temperature effects on the growth rate of bacteria and the stability of globular proteins. Journal of Theoretical Biology 2005, 233(3):351-362.
100. Ratkowsky D.A., Ross T., Macario N., Dommett T.W., Kamperman L. Choosing probability distributions for modelling generation time variability. Journal of Applied Bacteriology 1996, 80(2):131-137.
101. Rodionov D.G., Ishiguro E.E. Temperature sensitivity of bacteriolysis induced by lactam antibiotics in amino acid-deprived Escherichia coli. Journal of Bacteriology 1998, 180(8):2224-2227.
102. Rolfe M.D., Rice C.J., Lucchini S., Pin C., Thompson A., Cameron A.D.S., et al. Lag phase is a distinct growth phase that prepares bacteria for exponential growth and involves transient metal accumulation. Journal of Bacteriology 2012, 194(3):686-701.
103. Ross T. Bělehradék-type models. Journal of Industrial Microbiology 1993, 12(3-5):180-189.
104. Ross T., Dalgaard P. Secondary models. Modeling microbial responses in foods 2004, 63-150. CRC Press, Boca Raton. R.C. McKellar, X. Lu (Eds.).
105. Ross T., Olley J., McMeekin T.A., Ratkowsky D.A. Some comments on Huang, L (2010). Growth kinetics of Escherichia coli O157:H7 in mechanically-tenderized beef. International Journal of Food Microbiology, 140: 40-48. International Journal of Food Microbiology 2011, 147(1):78-80.
106. Ross T., Olley J., McMeekin T.A., Ratkowsky D.A. Reply to: response to letter to the editor: growth kinetics of Escherichia coli O157:H7 in mechanically tenderized beef. International Journal of Food Microbiology, 140: 40-48. International Journal of Food Microbiology 2011, 147(1):83-84.
107. Rosso L., Lobry J.R., Bajard S., Flandrois J.P. Convenient model to describe the combined effects of temperature and pH on microbial growth. Applied and Environmental Microbiology 1995, 61(2):610-616.
108. Rosso L., Lobry J.R., Flandrois J.P. An unexpected correlation between cardinal temperatures of microbial-growth highlighted by a new model. Journal of Theoretical Biology 1993, 162(4):447-463.
109. Rothman J.E., Shekman R. Molecular mechanism of protein folding in the cell. Cell 2011, 146(6):851-854.
110. Rowe W., Wedge D.C., Platt M., Kell D.B., Knowles J. Predictive models for population performance on real biological fitness landscapes. Bioinformatics 2010, 26(17):2145-2152.
111. Sarubbi E., Rudd K.E., Cashel M. Basal ppGpp level adjustment shown by new spot mutants affect steady-state growth rates and ribosomal RNA ribosomal promoter regulation in Escherichia coli. Molecular & General Genetics 1988, 213(2-3):214-222.
112. Schaechter M. From growth physiology to systems biology. International Microbiology 2006, 9(3):157-161.
113. Schaechter M., Maaløe O., Kjeldgaard N.O. Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. Journal of General Microbiology 1958, 19(3):592-606.
114. Schroeder B.O., Wu Z., Nuding S., Groscurth S., Marcinowski M., Beisner J., et al. Reduction of disulphide bonds unmasks potent antimicrobial activity of human beta-defensin 1. Nature 2011, 469(7330):419-423.
115. Shah D., Zhang Z.G., Khodursky A., Kaldalu N., Kurg K., Lewis K. Persisters: a distinct physiological state of E. coli. BMC Microbiology 2006, 6:53. 10.1186/1471-2180-6-53.
116. Shatalin K., Shatalina E., Mironov A., Nudler E. H(2)S: a universal defense against antibiotics in bacteria. Science 2011, 334(6058):986-990.
117. Silver L.L. A persistent problem. Journal of Medical Microbiology 2011, 60(3):267-268.
118. Smillie C.S., Smith M.B., Friedman J., Cordero O.X., David L.A., Alm E.J. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 2011, 480(7376):241-244.
119. Smith M.G. The generation time, lag time, and minimum temperature of growth of coliform organisms on meat, and the implications for codes of practice in abattoirs. Journal of Hygiene 1985, 94(3):289-300.
120. Sokurenko E.V., Gomulkiewicz R., Dykhuizen D.E. Opinion - source-sink dynamics of virulence evolution. Nature Reviews Microbiology 2006, 4(7):548-555.
121. Spencer R., Baines C.R. Effect of temperature on spoilage of wet white fish. I. Storage at constant temperatures between - 1° and 25°C. Food Technology 1964, 18(5):769-772.
122. Spoering A.L., Lewis K. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. Journal of Bacteriology 2001, 183(23):6746-6751.
123. Stecher B., Denzler R., Maier L., Bernet F., Sanders M.J., Pickard D.J., et al. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proceedings of the National Academy of Sciences 2012, 109(4):1269-1274.
124. Stockbridge R.B., Lewis C.A., Yuan Y., Wolfenden R. Impact of temperature on the time required for the establishment of primordial biochemistry, and for the evolution of enzymes. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(51):22102-22105.
125. Tittensor D.P., Mora C., Jetz W., Lotze H.K., Ricard D., Vanden Berghe E., et al. Global patterns and predictors of marine biodiversity across taxa. Nature 2010, 466(7310):1098-1107.
126. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459(7249):950-956.
127. Treangen T.J., Rocha E.P.C. Horizontal transfer, not duplication, drives the expansion of protein families in Prokaryotes. PLoS Genetics 2011, 7(1).
128. Van Derlinden E., Lule I., Bernaerts K., Van Impe J.F. Quantifying the heterogeneous heat response of Escherichia coli under dynamic temperatures. Journal of Applied Microbiology 2010, 108(4):1123-1135.
129. Vartoukian S.R., Palmer R.M., Wade W.G. Strategies for culture of 'unculturable' bacteria. FEMS Microbiology Letters 2010, 309(1):1-7.
130. Vieira-Silva S., Rocha E.P.C. The systemic imprint of growth and its uses in ecological (meta) genomics. PLoS Genetics 2010, 6(1):e1000808.
131. Vieira-Silva S., Touchon M., Abby S.S., Rocha E.P.C. Investment in rapid growth shapes the evolutionary rates of essential proteins. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(50):20030-20035.
132. Wang X., Wood T.K. Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response. Applied and Environmental Microbiology 2011, 77(16):5577-5583.
133. Wang M., Yafremava L.S., Caetano-Anolles D., Mittenthal J.E., Caetano-Anolles G. Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Research 2007, 17(11):1572-1585.
134. Whiting R.C., Buchanan R.L. A classification of models in predictive microbiology - reply. Food Microbiology 1993, 10(2):175-177.
135. de Wit R., Bouvier T. 'Everything is everywhere, but, the environment selects'; what did Baas Becking and Beijerinck really say?. Environmental Microbiology 2006, 8:755-758.
136. Yamaguchi Y., Inouye M. Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nature Reviews Microbiology 2011, 9(11):779-790.
137. Zhang Q.C., Lambert G., Liao D., Kim H., Robin K., Tung C.K., et al. Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 2011, 333(6050):1764-1767.