Induction of the Pho regulon suppresses the growth defect of an Escherichia coli sgrS mutant, connecting phosphate metabolism to the glucose-phosphate stress response

Journal of Bacteriology

Volumn 194, Issue 10, 2012, Pages 2520-2530

  Richards, Gregory R ^a   Vanderpool, Carin K ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; ALPHA METHYLGLUCOSIDE; BACTERIAL PROTEIN; GLUCOSE PHOSPHATE; MUTANT PROTEIN; PHOB PROTEIN; PHOSPHATE; PITA PROTEIN; SGRS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; GENE INDUCTION; GENE MUTATION; GROWTH INHIBITION; MICROARRAY ANALYSIS; NONHUMAN; PHOSPHATE METABOLISM; PRIORITY JOURNAL; REGULON; STRESS; TRANSCRIPTION INITIATION;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; MUTATION; PHOSPHATE TRANSPORT PROTEINS; PHOSPHATES; REGULON; RNA, BACTERIAL; STRESS, PHYSIOLOGICAL;

ESCHERICHIA COLI;

EID: 84861366998     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00009-12     Document Type: Article

References (68)

1. Amaral D, Kornberg HL. 1975. Regulation of fructose uptake by glucose in Escherichia coli. J. Gen. Microbiol. 90:157-168.
2. Amemura M, Makino K, Shinagawa H, Nakata A. 1990. Cross talk to the phosphate regulon of Escherichia coli by PhoM protein: PhoM is a histidine protein kinase and catalyzes phosphorylation of PhoB and PhoMopen reading frame 2. J. Bacteriol. 172:6300-6307.
3. Baba T, et al. 2006. Construction of Escherichia coli K-12 in-frame, singlegene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008. doi:10.1038/msb4100050.
4. Baek JH, Lee SY. 2006. Novel gene members of the Pho regulon of Escherichia coli. FEMS Microbiol. Lett. 264:104-109.
5. Barabote RD, Saier MH, Jr. 2005. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol. Mol. Biol. Rev. 69:608-634.
6. Beard SJ, et al. 2000. Evidence for the transport of zinc(II) ions via the pit inorganic phosphate transport system in Escherichia coli. FEMS Microbiol. Lett. 184:231-235.
7. Bertrand N, et al. 2010. Increased Pho regulon activation correlates with decreased virulence of an avian pathogenic Escherichia coli O78 strain. Infect. Immun. 78:5324-5331.
8. Brickman E, Beckwith J. 1975. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J. Mol. Biol. 96:307-316.
9. Crépin S, et al. 2011. The Pho regulon and the pathogenesis of Escherichia coli. Vet. Microbiol. 153:82-88.
10. Curtis SJ, Epstein W. 1975. Phosphorylation of D-glucose in Escherichia coli mutants defective in glucose phosphotransferase, mannose phosphotransferase, and glucokinase. J. Bacteriol. 122:1189-1199.
11. Deutscher J, Francke C, Postma PW. 2006. How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol. Mol. Biol. Rev. 70:939-1031.
12. Dozois CM, Daigle F, Curtiss R III. 2003. Identification of pathogenspecific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc. Natl. Acad. Sci. U. S. A. 100:247-252.
13. Ellermeier CD, Janakiraman A, Slauch JM. 2002. Construction of targeted single copy lac fusions using lambda Red and FLP-mediated sitespecific recombination in bacteria. Gene 290:153-161.
14. Englesberg E, et al. 1962. L-Arabinose-sensitive, L-ribulose 5-phosphate 4-epimerase-deficient mutants of Escherichia coli. J. Bacteriol. 84:137-146.
15. Farewell A, Kvint K, Nyström T. 1998. uspB, a new sigmaS-regulated gene in Escherichia coli which is required for stationary-phase resistance to ethanol. J. Bacteriol. 180:6140-6147.
16. Fukasawa T, Nikaido H. 1961. Galactose-sensitive mutants of Salmonella. II. Bacteriolysis induced by galactose. Biochim. Biophys. Acta 48:470-483.
17. Gottesman S, Storz G. 2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb. Perspect. Biol. 3(12):pii:a003798. doi:10.1101/cshperspect.a003798.
18. Harris RM, Webb DC, Howitt SM, Cox GB. 2001. Characterization of PitA and PitB from Escherichia coli. J. Bacteriol. 183:5008-5014.
19. Henderson PJ, Giddens RA, Jones-Mortimer MC. 1977. Transport ofgalactose, glucose and their molecular analogues by Escherichia coli K12. Biochem. J. 162:309-320.
20. Hoffer SM, Schoondermark P, van Veen HW, Tommassen J. 2001. Activation by gene amplification of pitB, encoding a third phosphate transporter of Escherichia coli K-12. J. Bacteriol. 183:4659-4663.
21. Hoffer SM, Tommassen J. 2001. The phosphate-binding protein of Escherichia coli is not essential for P(i)-regulated expression of the pho regulon. J. Bacteriol. 183:5768-5771.
22. Hogema BM, et al. 1998. Inducer exclusion by glucose 6-phosphate in Escherichia coli. Mol. Microbiol. 28:755-765.
23. Hogema BM, et al. 1998. Inducer exclusion in Escherichia coli by non-PTS substrates: the role of the PEP to pyruvate ratio in determining the phosphorylation state of enzyme IIAGlc. Mol. Microbiol. 30:487-498.
24. Hsieh YJ, Wanner BL. 2010. Global regulation by the seven-component Pi signaling system. Curr. Opin. Microbiol. 13:198-203.
25. Jackson RJ, et al. 2008. Expression of the PitA phosphate/metal transporter of Escherichia coli is responsive to zinc and inorganic phosphate levels. FEMS Microbiol. Lett. 289:219-224.
26. Kawamoto H, Koide Y, Morita T, Aiba H. 2006. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol. Microbiol. 61:1013-1022.
27. Keseler IM, et al. 2009. EcoCyc: a comprehensive view of Escherichia coli biology. Nucleic Acids Res. 37:D464-D470.
28. Kim SH, Schneider BL, Reitzer L. 2010. Genetics and regulation of the major enzymes of alanine synthesis in Escherichia coli. J. Bacteriol. 192: 5304-5311.
29. Kim SK, et al. 2000. Dual transcriptional regulation of the Escherichia coli phosphate-starvation-inducible psiE gene of the phosphate regulon by PhoB and the cyclic AMP (cAMP)-cAMP receptor protein complex. J. Bacteriol. 182:5596-5599.
30. Kimata K, Tanaka Y, Inada T, Aiba H. 2001. Expression of the glucose transporter gene, ptsG, is regulated at the mRNA degradation step in response to glycolytic flux in Escherichia coli. EMBO J. 20:3587-3595.
31. Kornberg A. 1995. Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J. Bacteriol. 177:491-496.
32. Kornberg H, Lambourne LT. 1994. The role of phosphoenolpyruvate in the simultaneous uptake of fructose and 2-deoxyglucose by Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 91:11080-11083.
33. Larsen RA, Wilson MM, Guss AM, Metcalf WW. 2002. Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch. Microbiol. 178:193-201.
34. Lee SJ, et al. 2009. Cellular stress created by intermediary metabolite imbalances. Proc. Natl. Acad. Sci. U. S. A. 106:19515-19520.
35. Lutz R, Bujard H. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res. 25:1203-1210.
36. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
37. Moreau PL. 2004. Diversion of the metabolic flux from pyruvate dehydrogenase to pyruvate oxidase decreases oxidative stress during glucose metabolism in nongrowing Escherichia coli cells incubated under aerobic, phosphate starvation conditions. J. Bacteriol. 186:7364-7368.
38. Morita T, El-Kazzaz W, Tanaka Y, Inada T, Aiba H. 2003. Accumulation of glucose 6-phosphate or fructose 6-phosphate is responsible for destabilization of glucose transporter mRNA in Escherichia coli. J. Biol. Chem. 278:15608-15614.
39. Morita T, Maki K, Aiba H. 2005. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev. 19:2176-2186.
40. Morita T, Mochizuki Y, Aiba H. 2006. Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc. Natl. Acad. Sci. U. S. A. 103:4858-4863.
41. Motomura K, et al. 2011. Overproduction of YjbB reduces the level of polyphosphate in Escherichia coli: a hypothetical role of YjbB in phosphate export and polyphosphate accumulation. FEMS Microbiol. Lett. 320:25-32.
42. Murray EL, Conway T. 2005. Multiple regulators control expression of the Entner-Doudoroff aldolase (Eda) of Escherichia coli. J. Bacteriol. 187: 991-1000.
43. Pogell BM, Maity BR, Frumkin S, Shapiro S. 1966. Induction of an active transport system for glucose 6-phosphate in Escherichia coli. Arch. Biochem. Biophys. 116:406-415.
44. Rephaeli AW, Saier MH, Jr. 1980. Substrate specificity and kinetic characterization of sugar uptake and phosphorylation, catalyzed by the mannose enzyme II of the phosphotransferase system in Salmonella typhimurium. J. Biol. Chem. 255:8585-8591.
45. Rice JB, Vanderpool CK. 2011. The small RNA SgrS controls sugarphosphate accumulation by regulating multiple PTS genes. Nucleic Acids Res. 39:3806-3819.
46. Richards GR, Vanderpool CK. 2011. Molecular call and response: the physiology of bacterial small RNAs. Biochim. Biophys. Acta 1809:525-531.
47. Rosenberg H, Gerdes RG, Chegwidden K. 1977. Two systems for the uptake of phosphate in Escherichia coli. J. Bacteriol. 131:505-511.
48. Sprague GF, Jr, Bell RM, Cronan JE, Jr. 1975. A mutant of Escherichia coli auxotrophic for organic phosphates: evidence for two defects in inorganic phosphate transport. Mol. Gen. Genet. 143:71-77.
49. Stock JB, Waygood EB, Meadow ND, Postma PW, Roseman S. 1982. Sugar transport by the bacterial phosphotransferase system. The glucose receptors of the Salmonella typhimurium phosphotransferase system. J. Biol. Chem. 257:14543-14552.
50. Storz G, Altuvia S, Wassarman KM. 2005. An abundance of RNA regulators. Annu. Rev. Biochem. 74:199-217.
51. Sun Y, Vanderpool CK. 2011. Regulation and function of Escherichia coli sugar efflux transporter A (SetA) during glucose-phosphate stress. J. Bacteriol. 193:143-153.
52. Tchieu JH, Norris V, Edwards JS, Saier MH, Jr. 2001. The complete phosphotranferase system in Escherichia coli. J. Mol. Microbiol. Biotechnol. 3:329-346.
53. Torriani A. 1990. From cell membrane to nucleotides: the phosphate regulon in Escherichia coli. Bioessays 12:371-376.
54. Vanderpool CK. 2007. Physiological consequences of small RNAmediated regulation of glucose-phosphate stress. Curr. Opin. Microbiol. 10:146-151.
55. Vanderpool CK, Gottesman S. 2004. Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol. Microbiol. 54:1076-1089.
56. Vanderpool CK, Gottesman S. 2007. The novel transcription factor SgrR coordinates the response to glucose-phosphate stress. J. Bacteriol. 189: 2238-2248.
57. van Veen HW, Abee T, Kortstee JJ, Konings WN, Zehnder JB. 1994. Translocation of metal phosphate via the phosphate inorganic transport system of Escherichia coli. Biochemistry 33:1766-1770.
58. Wadler CS, Vanderpool CK. 2007. A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc. Natl. Acad. Sci. U. S. A. 104: 20454-20459.
59. Wadler CS, Vanderpool CK. 2009. Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res. 37:5477-5485.
60. Wanner BL. 1993. Gene regulation by phosphate in enteric bacteria. J. Cell. Biochem. 51:47-54.
61. Wanner BL. 1983. Overlapping and separate controls on the phosphate regulon in Escherichia coli K12. J. Mol. Biol. 166:283-308.
62. Wanner BL. 1996. Phosphorous assimilation and control of the phosphate regulon, p 1357-1381. In Neidhardt FC et al. (ed), Escherichia coli and Salmonella: cellular and molecular biology, vol 1. ASM Press, Washington, DC.
63. Wanner BL, Latterell P. 1980. Mutants affected in alkaline phosphatase expression: evidence for multiple positive regulators of the phosphate regulon in Escherichia coli. Genetics 96:353-366.
64. Wanner BL, Wilmes-Riesenberg MR. 1992. Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J. Bacteriol. 174:2124-2130.
65. Waters LS, Storz G. 2009. Regulatory RNAs in bacteria. Cell 136:615-628.
66. Willsky GR, Bennett RL, Malamy MH. 1973. Inorganic phosphate transport in Escherichia coli: involvement of two genes which play a role in alkaline phosphatase regulation. J. Bacteriol. 113:529-539.
67. Willsky GR, Malamy MH. 1980. Characterization of two genetically separable inorganic phosphate transport systems in Escherichia coli. J. Bacteriol. 144:356-365.
68. Winkler HH. 1966. A hexose-phosphate transport system in Escherichia coli. Biochim. Biophys. Acta 117:231-240.