Evolution of penicillin-binding protein 2 concentration and cell shape during a long-term experiment with Escherichia coli

Journal of Bacteriology

Volumn 191, Issue 3, 2009, Pages 909-921

  Philippe, Nadège ^a,b   Pelosi, Ludovic ^a,b,d   Lenski, Richard E ^c   Schneider, Dominique ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b CNRS   (France)

^c Michigan State University ^*  (United States)

^d CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PENICILLIN BINDING PROTEIN 2; PENICILLIN BINDING PROTEIN A; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CELL SHAPE; CELL STRESS; CELL STRUCTURE; CELL VOLUME; ESCHERICHIA COLI; GENE INSERTION SEQUENCE; GENE MUTATION; MOLECULAR EVOLUTION; NONHUMAN; OSMOTIC STRESS; PHENOTYPE; PRIORITY JOURNAL; CYTOLOGY; GENETICS; METABOLISM; MUTATION; OPERON;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTATION; OPERON; PENICILLIN-BINDING PROTEINS; PEPTIDOGLYCAN;

EID: 63449114338     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01419-08     Document Type: Article

References (84)

1. Åkerlund, T., K. Nordström, and R. Bernander. 1995. Analysis of cell size and DNA content in exponentially growing and stationary-phase batch cultures of Escherichia coli. J. Bacteriol. 177:6791-6797.
2. Asoh, S., H. Matsuzawa, F. Ishino, J. L. Strominger, M. Matsuhashi, and T. Ohta. 1986. Nucleotide sequence of the pbpA gene and characteristics of the deduced amino acid sequence of penicillin-binding protein 2 of Escherichia coli K12. Eur. J. Biochem. 160:231-238.
3. Bass, S., Q. Gu, and A. Christen. 1996. Multicopy suppressors of Pre mutant Escherichia coli include two HtrA (DegP) protease homologs (HhoAB), DksA, and a truncated RlpA. J. Bacteriol. 178:1154-1161.
4. Begg, K. J., and W. D. Donachie. 1985. Cell shape and division in Escherichia coli: experiments with shape and division mutants. J. Bacteriol. 163:615-622.
5. Begg, K. J., and W. D. Donachie. 1998. Division planes alternate in spherical cells of Escherichia coli. J. Bacteriol. 180:2564-2567.
6. Bertsche, U., T. Kast, B. Wolf, C. Fraipont, M. E. G. Aarsman, K. Kannenberg, M. von Rechenberg, M. Nguyen-Distèche, T. den Blaauwen, J.-V. Höltje, and W. Vollmer. 2006. Interaction between two murein (peptidogly-can) synthases, PBP3 and PBP1B, in Escherichia coli. Mol. Microbiol. 61: 675-690.
7. Blasco, B., A. G. Pisabarro, and M. A. De Pedro. 1988. Peptidoglycan biosynthesis in stationary-phase cells of Escherichia coli. J. Bacteriol. 170:5224-5228.
8. Bledig, S. A., T. M. Ramseier, and M. H. Saier, Jr. 1996. FruR mediates catabolite activation of pyruvate kinase (pykF) gene expression in Escherichia coli. J. Bacteriol. 178:280-283.
9. Blount, Z. D., C. Z. Borland, and R. E. Lenski. 2008. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl. Acad. Sci. USA 105:7899-7906.
10. Botta, G. A., and J. T. Park. 1981. Evidence for involvement of penicillin binding protein 3 in murein synthesis during septation but not during cell elongation. J. Bacteriol. 145:333-340.
11. Cooper, T. F., D. E. Rozen, and R. E. Lenski. 2003. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc. Natl. Acad. Sci. USA 100:1072-1077.
12. Cooper, V. S., D. Schneider, M. Blot, and R. E. Lenski. 2001. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J. Bacterid. 183:2834-2841.
13. Cooper, V. S., and R. E. Lenski, 2000. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407:736-739.
14. Crozat, E., N. Philippe, R. E. Lenski, J. Geiselmann, and D. Schneider. 2005. Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics 169:523-532.
15. Dekel, E., and U. Alon. 2005. Optimality and evolutionary tuning of the expression level of a protein. Nature 436:588-592.
16. de la Rosa, E. J., M. A. de Pedro, and D. Vazquez. 1985. Penicillin binding proteins: role in initiation of murein synthesis in Escherichia coli. Proc. Natl. Acad. Sci. USA 82:5632-5635.
17. Denome, S. A., P. K. Elf, T. A. Henderson, D. E. Nelson, and K. D. Young. 1999. Escherichia coli mutants lacking all possible combinations of eight penicillin binding proteins: viability, characteristics, and implications for peptidoglycan synthesis. J. Bacteriol. 181:3981- 3993.
18. de Pedro, M. A., W. D. Donachie, J. V. Holtje, and H. Schwarz. 2001. Constitutive septal murein synthesis in Escherichia coli with impaired activity of the morphogenetic proteins RodA and penicillin-binding protein 2. J. Bacteriol. 183:4115-4126.
19. de Pedro, M. A, J. C. Quintala, J. V. Höltje, and H. Schwartz. 1997. Murein segregation in Escherichia coli. J. Bacteriol. 179:2823-2834.
20. Divakaruni, A. V., R. R. Ogorzalek Loo, Y. Xie, J. A. Loo, and J. W. Gober. 2005. The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 102:18602-18607.
21. Dougherty, T. J., K. Kennedy, R. E. Kessler, and M. J. Pucci. 1996. Direct quantitation of the number of individual penicillin-binding proteins per cell in Escherichia coli. J. Bacteriol. 178:6110- 6115.
22. Dykhuizen, D. 1978. Selection for tryptophan auxotrophs of Escherichia coli in glucose-limited chemostats as a test of the energy conservation hypothesis of evolution. Evolution 32:125-150.
23. Figge, R. M-, A. V. Divakaruni, and J. W. Gober. 2004. MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51:1321-1332.
24. Goffin, C, and J. M. Ghuysen. 1998. Multinodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:1079-1093.
25. Grana, M., and L. Acerenza. 2001. A model combining cell physiology and population genetics to explain Escherichia coli laboratory evolution. BMC Evol. Biol. 1:12.
26. Grose, J, H., U. Bergthorsson, and J. R. Roth. 2005. Regulation of NAD biosynthesis by the trifunctional NadR protein of Salmonella enterica. J. Bacteriol. 187:2774-2782.
27. Huisman, G. W., D. A. Siegele, M. M. Zambrano, and R. Kolter. 1996. Morphological and physiological changes during stationary phase, p. 1672-1682. In F. C. Neidhardt. R. Curtiss 111, J. L. lngraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology. 2nd ed. ASM Press. Washington, DC.
28. Ishino, F., W. Park, S. Tomioka, S. Tamaki, I. Takase, K. Kunugita, H. Matsuzawa, S. Asoh, T. Ohta, and B. G. Spratt. 1986. Peptidoglycan synthetic activities in membranes of Escherichia coli caused by overproduction of penicillin-binding protein 2 and RodA protein. J. Biol. Chem. 261:7024-7031.
29. James, R., J. Y, Haga, and A. B. Pardee. 1975. Inhibition of an early event in the cell division cycle of Escherichia coli by EL1060. an amidinopenicillanic acid. J. Bacteriol. 122:1283-1292.
30. Kruse, T., J. Bork-Jensen, and K. Gerdes. 2005. The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol. Microbiol. 55:78-89.
31. Lederberg, S. 1966. Genetics of host-controlled restriction and modification of deoxyribonucleic acid in Escherichia coli. J. Bacteriol. 91:1029-1036.
32. Legaree, B. A., C. B. Adams, and A. J. Clarke. 2007. Overproduction of penicillin-binding protein 2 and its inactive variants causes morphological changes and lysis in Escherichia coli. J. Bacteriol. 189:4975-4983.
33. Lenski, R. E. 2004. Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli. Plant Breed. Rev. 24:225-265.
34. Lenski, R. E., C. L. Winkworth, and M. A Riley. 2003. Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. J. Mol. Evol. 56:498-508.
35. Lenski, R. E., and J. A, Mongold. 2000. Cell size, shape, and fitness in evolving populations of bacteria, p. 221-235. In J. H. Brown and G. B. West (ed.). Scaling in biology. Oxford University Press. Oxford, United Kingdom.
36. Lenski, R. E., and M. Travisano. 1994. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc. Natl. Acad. Sci. USA 91:6808-6814.
37. Lenski, R. E-, J. A. Mongold, P. D. Sniegowski, M. Travisano, F. Vasi, P. J. Gerrish, and T. Schmidt. 1998. Evolution of competitive fitness in experimental populations of E. coli: what makes one genotype a better competitor than another? Antonie van Leeuwenhoek 73:35-47.
38. Lenski, R. E., M. R. Rose, S. C. Simpson, and S. C. Tadler. 1991. Long-term experimental evolution in Escherichia coli. 1. Adaptation and divergence during 2000 generations. Am. Nat. 138:1315-1341.
39. Link, A. J,, D, Phillips, and G. M. Church. 1997. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J. Bacteriol. 179:6228-6237.
40. Macheboeuf, P., C. Contreras-Martel, V. Job, O. Dideberg, and A. Dessen. 2006. Penicillin binding proteins: key players in bacterial cell cycle and drug resistance processes. FEMS Microbiol. Rev. 30:673-691.
41. McPherson, D. C., and D. L. Popham. 2003. Peptidoglycan synthesis in the absence of class A penicillin-binding proteins in Bacillus, subtilis. J. Bacteriol. 185:1423-1431.
42. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press. Cold Spring Harbor. NY.
43. Mongold, J. A., and R. E. Lenski. 1996. Experimental rejection of a non-adaptive explanation for increased cell size in Escherichia coli. J. Bacteriol. 178:5333-5334.
44. Nelson, D. E., and K. D. Young. 2001. Contributions of PBP 5 and dd-carboxypeptidase penicillin binding proteins to maintenance of cell shape in Escherichia coli. J. Bacteriol. 183:3055-3064.
45. Nelson, D. E., and K. D. Young. 2000. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J. Bacteriol. 182: 1714-1721.
46. Novak, M., T. Pfeiffer, R. E. Lenski, U. Sauer, and S. Bonhoeffer. 2006. Experimental tests for an evolutionary trade-off between growth rate and yield in E. coli. Am. Nat. 168:242-251.
47. Ostrowski, E. A., R. J. Woods, and R. E. Lenski. 2008. The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli. Proc. R. Soc. Lond. B 275:277-284.
48. Papadopoulos, D., D. Schneider, J. Meier-Eiss, W. Arber, R. E. Lenski, and M. Blot. 1999. Genomic evolution during a 10,000-generation experiment with bacteria. Proc. Natl. Acad. Sci. USA 96:3807-3812.
49. Pedersen, K,, and K. Gerdes. 1999. Multiple hok genes on the chromosome of Escherichia coli. Mol. Microbiol. 32:1090-1102.
50. Pelosi, L., L, Kuhn, D. Guetta, J, Garin, J. Geiselmann, R. E. Lenski, and D. Schneider. 2006. Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173:1851-1869.
51. Pepper, E. D., M. J. Farrell, and S. E. Finkel 2006. Role of penicillin-binding protein lb in competitive stationary phase survival of Escherichia coli. FEMS Microbiol. Lett. 263:61-67.
52. Philippe, N., E. Crozat, R. E. Lenski, and D. Schneider. 2007. Evolution of global regulatory networks during a long-term experiment with Escherichia coli. BioEssays 29:846-860.
53. Popham, D. L., and K. D. Young. 2003. Role of penicillin-binding proteins in bacterial cell morphogenesis. Curr. Opin. Microbiol. 6:594-599.
54. Powell, B. S., D. L. Court, Y. Nakamura, M. P. Rivas, and C. L. Turnbough, Jr. 1994. Rapid confirmation of single copy lambda prophage integration by PCR. Nucleic Acids Res. 22:5765-5766.
55. Romeis, T., and J. V. Höltje. 1994. Specific interaction of penicillin-binding proteins 3 and 7/8 with soluble lytic transglycosylase in Escherichia coli. J. Biol. Chem. 269:21603-21607.
56. Salgado, H., S. Gama-Castro, M. Paralta-Gil, E. Diaz-Peredo, F. Sanchez-Solano, A. Santos-Zavaleta, I. Martinez-Flores, V. Jimenez-Jacinto, C. Bonav ides-Martinez, J. Segura-Salazar, A. Martinez-Antonio, and J. Col-lado-Vides. 2006. RegulonDB (version 5.0): Escherichia coli K-12 transcriptional regulatory network, operon organization, and growth conditions. Nucleic Acids Res 34:D394-397.
57. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plain-view, NY.
58. Schaechter, M., O. Maaløe, and N. O. Kjelgaard. 1958. Dependence on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19:592-606.
59. Schiffer, G., and J. V. Höltje. 1999. Cloning and characterization of PBP 1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli. J. Biol. Chem. 274:32031-32039.
60. Schneider, D., E. Duperchy, J. Depeyrot, E. Coursange, R. E. Lenski, and M. Blot. 2002. Genomic comparisons among Escherichia coli strains B, K-12, and 0157:H7 using IS elements as molecular markers. BMC Microbiol. 2:18.
61. Schneider, D., E. Duperchy, E. Coursange, R. E. Lenski, and M. Blot. 2000. Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. Genetics 156:477-488.
62. Shaver, A. C, P. G. Dombrowski, J. Y. Sweeney, T. Treis, R. M. Zappala, and P. D. Sniegowski. 2002. Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics 162:557-566.
63. Simons, R. W., F. Houman, and N. Kleckner. 1987. Improved single and ulticopy lac-based cloning vectors for protein and Operon fusions. Gene 53:85-96"
64. Sniegowski, P. D., P. J. Gerrish, and R. E. Lenski. 1997. Evolution of high mutation rates in experimental populations of Escherichia coli. Nature 387: 703-705.
65. Spratt, B. G. 1975. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl. Acad. Sei. USA 72:2999-3003.
66. Spratt, B. G. 1977. The mechanism of action of mecillinam. J. Antimicrob. Chemother. 3(Suppl. B):13-19.
67. Spratt, B. G. 1977. Properties of the penicillin-binding proteins of Escherichia coli K12. Eur. J. Biochem. 72:341-352.
68. Spratt, B. G., and A. B. Pardee. 1975. Penicillin-binding proteins and cell shape in E. coli. Nature 254:516-517.
69. Takase, I., F. Ishino, M. Wachi, H. Kamata, M. Doi, S. Asoh, H. Matsuzawa, T. Ohta, and M. Matsuhashi. 1987. Genes encoding two lipoproteins in the leuS-dacA region of the Escherichia coli chromosome. J. Bacteriol. 169:5692-5699.
70. Travisano, M., and R. E. Lenski. 1996. Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics 143:15-26.
71. Tuomanen, E., and R. Cozens. 1987. Changes in peptidoglycan composition and penicillin-binding proteins in slowly growing Escherichia coli. J. Bacte-riol. 169:5308-5310. "
72. Uehara, T., and J, T. Park. 2002. Role of the murein precursor UDP-N-acetylmuramyl-L-Ala-γ-D-Glu-meso-diaminopimelic acid-D-Ala-D-Ala in repression of β-lactamase induction in cell division mutants. J, Bacteriol. 184:4233-4239.
73. van den Ent, F., M. Leaver, F. Bendezu, J. Errington, P. de Boer, and J. Löwe. 2006. Dimeric structure of the cell shape protein MreC and its functional implications. Mol. Microbiol. 62:1631-1642.
74. Vasi, F., M. Travisano, and R. E. Lenski. 1994. Long-term experimental evolution in Escherichia coli. 11. Changes in life-history traits during adaptation to a seasonal environment. Am. Nat. 144:432-456.
75. Vinella, D., D. Joseleau-Petit, D. Thevenet, P. Bouloc, and R. D'Ari, 1993. Penicillin-binding protein 2 inactivation in Escherichia coli results in cell division inhibition, which is relieved by FtsZ overexpression. J. Bacteriol. 175:6704-6710.
76. Vinella, D., R. D'Ari, A. Jaffe, and P. Bouloc. 1992. Penicillin binding protein 2 is dispensable in Escherichia coli when ppGpp synthesis is induced. EMBO J. 11:1493-1501.
77. Vollmer, W., M. von Rechenberg, and J. V. Höltje. 1999. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J. Biol." Chem. 274:6726-6734.
78. Weidel, W., and H. Pelzer. 1964. Bagshaped macromolecules-a new outlook on bacterial cell walls. Adv. Enzymol. 26:193-232.
79. Woods, R., D. Schneider, C. L. Winkworth, M. A. Riley, and R. E. Lenski. 2006. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc. Natl. Acad. Sci. USA 103:9107-9112.
80. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
81. Young, K. D. 2001. Approaching the physiological functions of penicillin-binding proteins in Escherichia coli. Biochimie 83:99-102.
82. Young, K. D. 2003. Bacterial shape. Mol. Microbiol. 49:571-580.
83. Yousif, S. Y., J. K. Broome-Smith, and B. G. Spratt. 1985. Lysis of Escherichia coli by β-lactam antibiotics: deletion analysis of the role of penicillin binding proteins 1A and IB. J. Gen. Microbiol." 131:2839-2845.
84. Zinser, E. R., and R. Kolter. 1999. Mutations enhancing amino acid catab-olism confer a growth advantage in stationary phase. J. Bacteriol. 181:5800-5807.