A Moonlighting Enzyme Links Escherichia coli Cell Size with Central Metabolism

PLoS Genetics

Volumn 9, Issue 7, 2013, Pages

  Hill, Norbert S ^a   Buske, Paul J ^a   Shi, Yue ^a   Levin, Petra Anne ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; FTSZ PROTEIN; GLUCOSYLTRANSFERASE; OPGH PROTEIN; POLYMER; TUBULIN; UGTP PROTEIN; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCOSE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL METABOLISM; CELL DIVISION; CELL SIZE; CONTROLLED STUDY; CONVERGENT EVOLUTION; ENZYME ACTIVITY; ESCHERICHIA COLI; GROWTH REGULATION; NONHUMAN; NUTRIENT AVAILABILITY; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL DIVISION; CELL SIZE; CYTOSKELETAL PROTEINS; ESCHERICHIA COLI; GLUCOSYLTRANSFERASES; URIDINE DIPHOSPHATE GLUCOSE;

EID: 84880834788     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003663     Document Type: Article

References (76)

1. Chien AC, Hill NS, Levin PA, (2012) Cell size control in bacteria. Curr Biol 22: R340-349.
2. Schaechter M, Maaløe O, Kjeldgaard NO, (1958) Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. J Gen Microbiol 19: 592-606.
3. Pierucci O, Helmstetter CE, Rickert M, Weinberger M, Leonard AC, (1987) Overexpression of the dnaA gene in Escherichia coli B/r: chromosome and minichromosome replication in the presence of rifampin. J Bacteriol 169: 1871-1877.
4. Sargent MG, (1975) Control of cell length in Bacillus subtilis. J Bacteriol 123: 7-19.
5. Fantes P, Nurse P, (1977) Control of cell size at division in fission yeast by a growth-modulated size control over nuclear division. Exp Cell Res 107: 377-386.
6. Weart RB, Lee AH, Chien AC, Haeusser DP, Hill NS, et al. (2007) A metabolic sensor governing cell size in bacteria. Cell 130: 335-347.
7. Chien AC, Zareh SK, Wang YM, Levin PA, (2012) Changes in the oligomerization potential of the division inhibitor UgtP co-ordinate Bacillus subtilis cell size with nutrient availability. Mol Microbiol 86: 594-610.
8. Lazarevic V, Soldo B, Medico N, Pooley H, Bron S, et al. (2005) Bacillus subtilis alpha-phosphoglucomutase is required for normal cell morphology and biofilm formation. Appl Environ Microbiol 71: 39-45.
9. Lu M, Kleckner N, (1994) Molecular cloning and characterization of the pgm gene encoding phosphoglucomutase of Escherichia coli. J Bacteriol 176: 5847-5851.
10. Hill NS, Kadoya R, Chattoraj DK, Levin PA, (2012) Cell size and the initiation of DNA replication in bacteria. PLoS Genet 8: e1002549.
11. Lu M, Campbell J, Boye E, Kleckner N, (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77: 413-426.
12. Hale CA, de Boer PA, (1999) Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J Bacteriol 181: 167-176.
13. Bernhardt TG, de Boer PA, (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 18: 555-564.
14. Ricard M, Hirota Y, (1973) Process of cellular division in Escherichia coli: physiological study on thermosensitive mutants defective in cell division. J Bacteriol 116: 314-322.
15. Lutkenhaus JF, Wu HC, (1980) Determination of transcriptional units and gene products from the ftsA region of Escherichia coli. J Bacteriol 143: 1281-1288.
16. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006 0008.
17. Breton C, Snajdrova L, Jeanneau C, Koca J, Imberty A, (2006) Structures and mechanisms of glycosyltransferases. Glycobiology 16: 29R-37R.
18. Bohin JP, (2000) Osmoregulated periplasmic glucans in Proteobacteria. FEMS Microbiol Lett 186: 11-19.
19. Schneider JE, Reinhold V, Rumley MK, Kennedy EP, (1979) Structural studies of the membrane-derived oligosaccharides of Escherichia coli. J Biol Chem 254: 10135-10138.
20. Hanoulle X, Rollet E, Clantin B, Landrieu I, Odberg-Ferragut C, et al. (2004) Structural analysis of Escherichia coli OpgG, a protein required for the biosynthesis of osmoregulated periplasmic glucans. J Mol Biol 342: 195-205.
21. Rajagopal S, Eis N, Bhattacharya M, Nickerson KW, (2003) Membrane-derived oligosaccharides (MDOs) are essential for sodium dodecyl sulfate resistance in Escherichia coli. FEMS Microbiol Lett 223: 25-31.
22. Ebel W, Vaughn GJ, Peters HK 3rd, Trempy JE, (1997) Inactivation of mdoH leads to increased expression of colanic acid capsular polysaccharide in Escherichia coli. J Bacteriol 179: 6858-6861.
23. Fiedler W, Rotering H, (1988) Properties of Escherichia coli mutants lacking membrane-derived oligosaccharides. J Biol Chem 263: 14684-14689.
24. Girgis HS, Liu Y, Ryu WS, Tavazoie S, (2007) A comprehensive genetic characterization of bacterial motility. PLoS Genet 3: 1644-1660.
25. Holtje JV, Fiedler W, Rotering H, Walderich B, van Duin J, (1988) Lysis induction of Escherichia coli by the cloned lysis protein of the phage MS2 depends on the presence of osmoregulatory membrane-derived oligosaccharides. J Biol Chem 263: 3539-3541.
26. Penaloza-Vazquez A, Sreedharan A, Bender CL, (2010) Transcriptional studies of the hrpM/opgH gene in Pseudomonas syringae during biofilm formation and in response to different environmental challenges. Environ Microbiol 12: 1452-1467.
27. Loubens I, Debarbieux L, Bohin A, Lacroix JM, Bohin JP, (1993) Homology between a genetic locus (mdoA) involved in the osmoregulated biosynthesis of periplasmic glucans in Escherichia coli and a genetic locus (hrpM) controlling pathogenicity of Pseudomonas syringae. Mol Microbiol 10: 329-340.
28. Page F, Altabe S, Hugouvieux-Cotte-Pattat N, Lacroix JM, Robert-Baudouy J, et al. (2001) Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity. J Bacteriol 183: 3134-3141.
29. Bhagwat AA, Jun W, Liu L, Kannan P, Dharne M, et al. (2009) Osmoregulated periplasmic glucans of Salmonella enterica serovar Typhimurium are required for optimal virulence in mice. Microbiology 155: 229-237.
30. Gottesman S, McCullen CA, Guillier M, Vanderpool CK, Majdalani N, et al. (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71: 1-11.
31. Shiba Y, Matsumoto K, Hara H, (2006) DjlA negatively regulates the Rcs signal transduction system in Escherichia coli. Genes Genet Syst 81: 51-56.
32. Gervais FG, Phoenix P, Drapeau GR, (1992) The rcsB gene, a positive regulator of colanic acid biosynthesis in Escherichia coli, is also an activator of ftsZ expression. J Bacteriol 174: 3964-3971.
33. Carballes F, Bertrand C, Bouche JP, Cam K, (1999) Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB. Mol Microbiol 34: 442-450.
34. Ward JE Jr, Lutkenhaus J, (1985) Overproduction of FtsZ induces minicell formation in E. coli. Cell 42: 941-949.
35. Hengge R, (2008) The two-component network and the general stress sigma factor RpoS (sigma S) in Escherichia coli. Adv Exp Med Biol 631: 40-53.
36. Bohringer J, Fischer D, Mosler G, Hengge-Aronis R, (1995) UDP-glucose is a potential intracellular signal molecule in the control of expression of sigma S and sigma S-dependent genes in Escherichia coli. J Bacteriol 177: 413-422.
37. Nagahama H, Sakamoto Y, Matsumoto K, Hara H, (2006) RcsA-dependent and-independent growth defects caused by the activated Rcs phosphorelay system in the Escherichia coli pgsA null mutant. J Gen Appl Microbiol 52: 91-98.
38. Cano DA, Dominguez-Bernal G, Tierrez A, Garcia-Del Portillo F, Casadesus J, (2002) Regulation of capsule synthesis and cell motility in Salmonella enterica by the essential gene igaA. Genetics 162: 1513-1523.
39. Debarbieux L, Bohin A, Bohin JP, (1997) Topological analysis of the membrane-bound glucosyltransferase, MdoH, required for osmoregulated periplasmic glucan synthesis in Escherichia coli. J Bacteriol 179: 6692-6698.
40. Weart RB, Nakano S, Lane BE, Zuber P, Levin PA, (2005) The ClpX chaperone modulates assembly of the tubulin-like protein FtsZ. Mol Microbiol 57: 238-249.
41. Mukherjee A, Lutkenhaus J, (1999) Analysis of FtsZ assembly by light scattering and determination of the role of divalent metal cations. J Bacteriol 181: 823-832.
42. Buske PJ, Levin PA, (2012) Extreme C terminus of bacterial cytoskeletal protein FtsZ plays fundamental role in assembly independent of modulatory proteins. J Biol Chem 287: 10945-10957.
43. Cho H, McManus HR, Dove SL, Bernhardt TG, (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci U S A 108: 3773-3778.
44. Hu Z, Mukherjee A, Pichoff S, Lutkenhaus J, (1999) The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci U S A 96: 14819-14824.
45. Sugimoto S, Yamanaka K, Nishikori S, Miyagi A, Ando T, et al. (2010) AAA+ chaperone ClpX regulates dynamics of prokaryotic cytoskeletal protein FtsZ. J Biol Chem 285: 6648-6657.
46. Mukherjee A, Cao C, Lutkenhaus J, (1998) Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc Natl Acad Sci U S A 95: 2885-2890.
47. Erickson HP, Anderson DE, Osawa M, (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74: 504-528.
48. Lutkenhaus J, Pichoff S, Du S, (2012) Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton (Hoboken).
49. Adams DW, Errington J, (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7: 642-653.
50. Romberg L, Levin PA, (2003) Assembly dynamics of the bacterial cell division protein FtsZ: poised at the edge of stability. Annu Rev Microbiol 57: 125-154.
51. Cordell SC, Robinson EJ, Lowe J, (2003) Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci U S A 100: 7889-7894.
52. Mukherjee A, Lutkenhaus J, (1998) Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J 17: 462-469.
53. Chen Y, Milam SL, Erickson HP, (2012) SulA inhibits assembly of FtsZ by a simple sequestration mechanism. Biochemistry 51: 3100-3109.
54. Shen B, Lutkenhaus J, (2010) Examination of the interaction between FtsZ and MinCN in E. coli suggests how MinC disrupts Z rings. Mol Microbiol 75: 1285-1298.
55. Thanbichler M, Shapiro L, (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126: 147-162.
56. Tonthat NK, Arold ST, Pickering BF, Van Dyke MW, Liang S, et al. (2011) Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30: 154-164.
57. Weart RB, Levin PA, (2003) Growth rate-dependent regulation of medial FtsZ ring formation. J Bacteriol 185: 2826-2834.
58. Palacios P, Vicente M, Sanchez M, (1996) Dependency of Escherichia coli cell-division size, and independency of nucleoid segregation on the mode and level of ftsZ expression. Mol Microbiol 20: 1093-1098.
59. Boyle DS, Khattar MM, Addinall SG, Lutkenhaus J, Donachie WD, (1997) ftsW is an essential cell-division gene in Escherichia coli. Mol Microbiol 24: 1263-1273.
60. Vats P, Shih YL, Rothfield L, (2009) Assembly of the MreB-associated cytoskeletal ring of Escherichia coli. Mol Microbiol 72: 170-182.
61. Huberts DH, van der Klei IJ, (2010) Moonlighting proteins: an intriguing mode of multitasking. Biochim Biophys Acta 1803: 520-525.
62. Kennedy EP, (1982) Osmotic regulation and the biosynthesis of membrane-derived oligosaccharides in Escherichia coli. Proc Natl Acad Sci U S A 79: 1092-1095.
63. Kennedy EP, Rumley MK, (1988) Osmotic regulation of biosynthesis of membrane-derived oligosaccharides in Escherichia coli. J Bacteriol 170: 2457-2461.
64. Wood JM, (1999) Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev 63: 230-262.
65. Meury J, (1988) Glycine betaine reverses the effects of osmotic stress on DNA replication and cellular division in Escherichia coli. Arch Microbiol 149: 232-239.
66. Bury-Mone S, Nomane Y, Reymond N, Barbet R, Jacquet E, et al. (2009) Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet 5: e1000651.
67. Varon D, Boylan SA, Okamoto K, Price CW, (1993) Bacillus subtilis gtaB encodes UDP-glucose pyrophosphorylase and is controlled by stationary-phase transcription factor sigma B. J Bacteriol 175: 3964-3971.
68. Zhang YM, Rock CO, (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6: 222-233.
69. Yao Z, Davis RM, Kishony R, Kahne D, Ruiz N, (2012) Regulation of cell size in response to nutrient availability by fatty acid biosynthesis in Escherichia coli. Proc Natl Acad Sci U S A 109: E2561-2568.
70. Clark DJ, Maaløe O, (1967) DNA replication and the division cycle in Escherichia coli. J Mol Biol 23: 99-112.
71. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
72. Levin PA (2002) Light Microscopy Techniques for Bacterial Cell Biology. In: Sansonetti PJ, Zychlinsky A, editors. Molecular Cellular Microbiology. London: Academic Press, Ltd. pp. 115-132.
73. Haeusser DP, Schwartz RL, Smith AM, Oates ME, Levin PA, (2004) EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ. Mol Microbiol 52: 801-814.
74. Ingerman E, Nunnari J, (2005) A continuous, regenerative coupled GTPase assay for dynamin-related proteins. Methods Enzymol 404: 611-619.
75. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
76. Tanabe M, Kanehisa M, (2012) Using the KEGG database resource. Curr Protoc Bioinformatics Chapter 1: Unit1 12.