Massive diversification in aging colonies of Escherichia coli

Journal of Bacteriology

Volumn 196, Issue 17, 2014, Pages 3059-3073

  Saint Ruf, Claude ^a   Garfa Traoré, Meriem ^a   Collin, Valérie ^b   Cordier, Corinne ^a   Franceschi, Christine ^b   Matic, Ivan ^a  

^a INSERM   (France)

^b BIOMÉRIEUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; FLUORESCENT DYE; SIGMA FACTOR RPOS;

AGING; ARTICLE; BACTERIAL MUTATION; BACTERIUM COLONY; BIOFILM; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; MORPHOLOGY; MUTATION RATE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; STRESS;

ADAPTATION, PHYSIOLOGICAL; BIODIVERSITY; BIOLOGICAL EVOLUTION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC FITNESS; PHENOTYPE; TIME FACTORS;

EID: 84905492667     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01421-13     Document Type: Article

References (80)

1. Rainey PB, Travisano M. 1998. Adaptive radiation in a heterogeneous environment. Nature 394: 69-72. http://dx.doi.org/10.1038/27900.
2. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T. 2006. Clonal adaptive radiation in a constant environment. Science 313: 514-517. http://dx.doi.org/10.1126/science.1129865.
3. MacLean RC. 2005. Adaptive radiation in microbial microcosms. J. Evol. Biol. 18: 1376-1386. http://dx.doi.org/10.1111/j.1420-9101.2005.00931.x.
4. Yachi S, Loreau M. 1999. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc. Natl. Acad. Sci. U. S. A. 96: 1463-1468. http://dx.doi.org/10.1073/pnas.96.4.1463.
5. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318.
6. Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95-108. http://dx.doi.org/10.1038/nrmicro821.
7. Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6: 199-210. http://dx.doi.org/10.1038/nrmicro1838.
8. Beloin C, Roux A, Ghigo JM. 2008. Escherichia coli biofilms. Curr. Top. Microbiol. Immunol. 322: 249-289. http://dx.doi.org/10.1007/978-3-540-75418-3_12.
9. Monds RD, O'Toole GA. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17:73-87. http://dx.doi.org/10.1016/j.tim.2008.11.001.
10. Shapiro JA. 1987. Organization of developing Escherichia coli colonies viewed by scanning electron microscopy. J. Bacteriol. 169:142-156.
11. Shapiro JA. 1995. The significances of bacterial colony patterns. Bioessays 17:597-607. http://dx.doi.org/10.1002/bies.950170706.
12. Peters AC, Wimpenny JW, Coombs JP. 1987. Oxygen profiles in, and in the agar beneath, colonies of Bacillus cereus, Staphylococcus albus and Escherichia coli. J. Gen. Microbiol. 133:1257-1263.
13. Asally M, Kittisopikul M, Rue P, Du Y, Hu Z, Cagatay T, Robinson AB, Lu H, Garcia-Ojalvo J, Suel GM. 2012. Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc. Natl. Acad. Sci. U. S. A. 109:18891-18896. http://dx.doi.org/10.1073/pnas.1212429109.
14. Serra DO, Richter AM, Klauck G, Mika F, Hengge R. 2013. Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. mBio 4 (2): e00103-13. http://dx.doi.org/10.1128/mBio.00103-13.
15. Knudsen GM, Nielsen MB, Grassby T, Danino-Appleton V, Thomsen LE, Colquhoun IJ, Brocklehurst TF, Olsen JE, Hinton JC. 2012. A third mode of surface-associated growth: immobilization of Salmonella enterica serovar Typhimurium modulates the RpoS-directed transcriptional programme. Environ. Microbiol. 14:1855-1875. http://dx.doi.org/10.1111/j.1462-2920.2012.02703.x.
16. Shapiro JA. 1998. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52:81-104. http://dx.doi.org/10.1146/annurev.micro.52.1.81.
17. Aguilar C, Vlamakis H, Losick R, Kolter R. 2007. Thinking about Bacillus subtilis as a multicellular organism. Curr. Opin. Microbiol. 10: 638-643. http://dx.doi.org/10.1016/j.mib.2007.09.006.
18. Robinson TP, Wimpenny JW, Earnshaw RG. 1991. pH gradients through colonies of Bacillus cereus and the surrounding agar. J. Gen. Microbiol. 137: 2885-2889. http://dx.doi.org/10.1099/00221287-137-12-2885.
19. Hadley P. 1927. Microbic dissociation. The instability of bacterial species with special reference to active dissociation and transmissible autolysis. Infect. Dis. 40:1-312.
20. Bjedov I, Tenaillon O, Gerard B, Souza V, Denamur E, Radman M, Taddei F, Matic I. 2003. Stress-induced mutagenesis in bacteria. Science 300:1404-1409. http://dx.doi.org/10.1126/science.1082240.
21. Boles BR, Singh PK. 2008. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc. Natl. Acad. Sci. U. S. A. 105:12503-12508. http://dx.doi.org/10.1073/pnas.0801499105.
22. Kolter R, Siegele DA, Tormo A. 1993. The stationary phase of the bacterial life cycle. Annu. Rev. Microbiol. 47:855-874. http://dx.doi.org/10.1146/annurev.mi.47.100193.004231.
23. Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R. 1993. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757-1760. http://dx.doi.org/10.1126/science.7681219.
24. King T, Ishihama A, Kori A, Ferenci T. 2004. A regulatory trade-offas a source of strain variation in the species Escherichia coli. J. Bacteriol. 186: 5614-5620. http://dx.doi.org/10.1128/JB.186.17.5614-5620.2004.
25. Tenaillon O, Skurnik D, Picard B, Denamur E. 2010. The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 8:207-217. http://dx.doi.org/10.1038/nrmicro2298.
26. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140. http://dx.doi.org/10.1038/nrmicro818.
27. Jarvis WR, Martone WJ. 1992. Predominant pathogens in hospital infections. J. Antimicrob. Chemother. 29(Suppl A):19-24. http://dx.doi.org/10.1093/jac/29.suppl_A.19.
28. Russo TA, Johnson JR. 2003. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect. 5:449-456. http://dx.doi.org/10.1016/S1286-4579(03)00049-2.
29. van Elsas JD, Semenov AV, Costa R, Trevors JT. 2011. Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J. 5:173-183. http://dx.doi.org/10.1038/ismej.2010.80.
30. Winfield MD, Groisman EA. 2003. Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl. Environ. Microbiol. 69:3687-3694. http://dx.doi.org/10.1128/AEM.69.7.3687-3694.2003.
31. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625. http://dx.doi.org/10.3201/eid0505.990502.
32. Grad YH, Lipsitch M, Feldgarden M, Arachchi HM, Cerqueira GC, Fitzgerald M, Godfrey P, Haas BJ, Murphy CI, Russ C, Sykes S, Walker BJ, Wortman JR, Young S, Zeng Q, Abouelleil A, Bochicchio J, Chauvin S, Desmet T, Gujja S, McCowan C, Montmayeur A, Steelman S, Frimodt-Moller J, Petersen AM, Struve C, Krogfelt KA, Bingen E, Weill FX, Lander ES, Nusbaum C, Birren BW, Hung DT, Hanage WP. 2012. Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc. Natl. Acad. Sci. U. S. A. 109:3065-3070. http://dx.doi.org/10.1073/pnas.1121491109.
33. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301: 105-107. http://dx.doi.org/10.1126/science.1084550.
34. Brown MR, Barker J. 1999. Unexplored reservoirs of pathogenic bacteria: protozoa and biofilms. Trends Microbiol. 7:46-50. http://dx.doi.org/10.1016/S0966-842X(98)01425-5.
35. Anderson GG, O'Toole GA. 2008. Innate and induced resistance mechanisms of bacterial biofilms. Curr. Top. Microbiol. Immunol. 322:85-105. http://dx.doi.org/10.1007/978-3-540-75418-3_5.
36. Schwartz DJ, Chen SL, Hultgren SJ, Seed PC. 2011. Population dynamics and niche distribution of uropathogenic Escherichia coli during acute and chronic urinary tract infection. Infect. Immun. 79:4250-4259. http://dx.doi.org/10.1128/IAI.05339-11.
37. Mulvey MA, Schilling JD, Hultgren SJ. 2001. Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect. Immun. 69:4572-4579. http://dx.doi.org/10.1128/IAI.69.7.4572-4579.2001.
38. Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474. http://dx.doi.org/10.1126/science.277.5331.1453.
39. Lindner AB, Madden R, Demarez A, Stewart EJ, Taddei F. 2008. Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl. Acad. Sci. U. S. A. 105:3076-3081. http://dx.doi.org/10.1073/pnas.0708931105.
40. Miller JH. 1992. A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
42. Fontaine F, Stewart EJ, Lindner AB, Taddei F. 2008. Mutations in two global regulators lower individual mortality in Escherichia coli. Mol. Microbiol. 67:2-14. http://dx.doi.org/10.1111/j.1365-2958.2007.05988.x.
43. Baba T, Mori H. 2008. The construction of systematic in-frame, singlegene knockout mutant collection in Escherichia coli K-12. Methods Mol. Biol. 416:171-181. http://dx.doi.org/10.1007/978-1-59745-321-9_11.
44. Maniatis T, Fritsch EF, Sambrook J. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
45. Shapiro HM. 2000. Membrane potential estimation by flow cytometry. Methods 21:271-279. http://dx.doi.org/10.1006/meth.2000.1007.
46. Saint-Ruf C, Cordier C, Megret J, Matic I. 2010. Reliable detection of dead microbial cells by using fluorescent hydrazides. Appl. Environ. Microbiol. 76:1674-1678. http://dx.doi.org/10.1128/AEM.02125-09.
47. Dajkovic A, Mukherjee A, Lutkenhaus J. 2008. Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization. J. Bacteriol. 190:2513-2526. http://dx.doi.org/10.1128/JB.01612-07.
48. Friedberg WG, Siede W, Wood RD, Schultz RA, Ellenberger T. 2006. DNA repair and mutagenesis, 2nd ed. ASM Press, Washington, DC.
49. Toomre D, Pawley JB. 2006. Disk-scanning confocal microscopy, p 221-230. In Pawley JB (ed), Handbook of biological confocal microscopy. Springer Science Business Media, New York, NY.
50. Han TH, Lee JH, Cho MH, Wood TK, Lee J. 2011. Environmental factors affecting indole production in Escherichia coli. Res. Microbiol. 162:108-116. http://dx.doi.org/10.1016/j.resmic.2010.11.005.
51. Tang YW, Ellis NM, Hopkins MK, Smith DH, Dodge DE, Persing DH. Comparison of phenotypic and genotypic techniques for identification of unusual aerobic pathogenic gram-negative bacilli. J. Clin. Microbiol. 36:3674-3679.
52. Diard M, Baeriswyl S, Clermont O, Gouriou S, Picard B, Taddei F, Denamur E, Matic I. 2007. Caenorhabditis elegans as a simple model to study phenotypic and genetic virulence determinants of extraintestinal pathogenic Escherichia coli. Microbes Infect. 9:214-223. http://dx.doi.org/10.1016/j.micinf.2006.11.009.
53. Chavant P, Gaillard-Martinie B, Talon R, Hebraud M, Bernardi T. A new device for rapid evaluation of biofilm formation potential by bacteria. J. Microbiol. Methods 68: 605-612. http://dx.doi.org/10.1016/j.mimet.2006.11.010.
54. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R. 2005. Genome- wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187:1591-1603. http://dx.doi.org/10.1128/JB.187.5.1591-1603.2005.
55. Lacour S, Landini P. 2004. SigmaS-dependent gene expression at the onset of stationary phase in Escherichia coli: function of sigmaS-dependent genes and identification of their promoter sequences. J. Bacteriol. 186:7186-7195. http://dx.doi.org/10.1128/JB.186.21.7186-7195.2004.
56. Patten CL, Kirchhof MG, Schertzberg MR, Morton RA, Schellhorn HE. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol. Genet. Genomics 272:580-591. http://dx.doi.org/10.1007/s00438-004-1089-2.
57. Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, Davison WM, Buckingham-Meyer K, Stewart PS. 2007. Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J. Bacteriol. 189:4223-4233. http://dx.doi.org/10.1128/JB.00107-07.
58. Kim J, Hahn JS, Franklin MJ, Stewart PS, Yoon J. 2009. Tolerance of dormant and active cells in Pseudomonas aeruginosa PA01 biofilm to antimicrobial agents. J. Antimicrob. Chemother. 63:129-135. http://dx.doi.org/10.1093/jac/dkn462.
59. Margolin W. 2001. Spatial regulation of cytokinesis in bacteria. Curr. Opin. Microbiol. 4:647-652. http://dx.doi.org/10.1016/S1369-5274(01)00264-8.
60. Delmas S, Matic I. 2005. Cellular response to horizontally transferred DNA in Escherichia coli is tuned by DNA repair systems. DNA Repair 4:221-229. http://dx.doi.org/10.1016/j.dnarep.2004.09.008.
61. Becker G, Klauck E, Hengge-Aronis R. 1999. Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc. Natl. Acad. Sci. U. S. A. 96:6439-6444. http://dx.doi.org/10.1073/pnas.96.11.6439.
62. Harfe BD, Jinks-Robertson S. 2000. DNA mismatch repair and genetic instability. Annu. Rev. Genet. 34:359-399. http://dx.doi.org/10.1146/annurev.genet.34.1.359.
63. Domka J, Lee J, Wood TK. 2006. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl. Environ. Microbiol. 72:2449-2459. http://dx.doi.org/10.1128/AEM.72.4.2449-2459.2006.
64. Lee HH, Molla MN, Cantor CR, Collins JJ. 2010. Bacterial charity work leads to population-wide resistance. Nature 467:82-85. http://dx.doi.org/10.1038/nature09354.
65. Garbe TR, Kobayashi M, Yukawa H. 2000. Indole-inducible proteins in bacteria suggest membrane and oxidant toxicity. Arch. Microbiol. 173: 78-82. http://dx.doi.org/10.1007/s002030050012.
66. Newton WA, Snell EE. 1965. Formation and interrelationships of tryptophanase and tryptophan synthetases in Escherichia coli. J. Bacteriol. 89:355-364.
67. Yanofsky C, Horn V, Gollnick P. 1991. Physiological studies of tryptophan transport and tryptophanase operon induction in Escherichia coli. J. Bacteriol. 173:6009-6017.
68. Hallatschek O, Nelson DR. 2010. Life at the front of an expanding population. Evolution 64:193-2006. http://dx.doi.org/10.1111/j.1558-5646.2009.00809.x.
69. Imlay JA. 1995. A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli. J. Biol. Chem. 270:19767-19777.
70. Tsui HC, Feng G, Winkler ME. 1997. Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12. J. Bacteriol. 179:7476-7487.
71. Gutierrez A, Laureti L, Crussard S, Abida H, Rodriguez-Rojas A, Blazquez J, Baharoglu Z, Mazel D, Darfeuille F, Vogel J, Matic I. 2013. beta-lactam antibiotics promote bacterial mutagenesis via an RpoSmediated reduction in replication fidelity. Nat. Commun. 4:1610. http://dx.doi.org/10.1038/ncomms2607.
72. Rosenzweig RF, Sharp RR, Treves DS, Adams J. 1994. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137:903-917.
73. Brightman V, Martin WR. 1961. Pathway for the dissimilation of itaconic and mesaconic acids. J. Bacteriol. 82:376-382.
74. Wolfe AJ. 2005. The acetate switch. Microbiol. Mol. Biol. Rev. 69:12-50. http://dx.doi.org/10.1128/MMBR.69.1.12-50.2005.
75. Furmanski P, Wegener WS, Reeves HC, Ajl SJ. 1967. Function of the glyoxylate-condensing enzymes. I. Growth of Escherichia coli on n-valeric acid. J. Bacteriol. 94:1075-1081.
76. Wegener WS, Furmanski P, Ajl SJ. 1967. Selection of mutants constitutive for several glyoxylate condensing enzymes during growth on valeric acid. Biochim. Biophys. Acta 144:34-50. http://dx.doi.org/10.1016/0005-2760(67)90075-6.
77. McKinney JD, Honer zu Bentrup K, Munoz-Elias EJ, Miczak A, Chen B, Chan WT, Swenson D, Sacchettini JC, Jacobs WR, Jr, Russell DG. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735-738. http://dx.doi.org/10.1038/35021074.
78. Munoz-Elias EJ, McKinney JD. 2005. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat. Med. 11:638-644. http://dx.doi.org/10.1038/nm1252.
79. Lorenz MC, Fink GR. 2001. The glyoxylate cycle is required for fungal virulence. Nature 412:83-86. http://dx.doi.org/10.1038/35083594.
80. Lindsey TL, Hagins JM, Sokol PA, Silo-Suh LA. 2008. Virulence determinants from a cystic fibrosis isolate of Pseudomonas aeruginosa include isocitrate lyase. Microbiology 154:1616-1627. http://dx.doi.org/10.1099/mic.0.2007/014506-0.