Correcting direct effects of ethanol on translation and transcription machinery confers ethanol tolerance in bacteria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 25, 2014, Pages

  Haft, Rembrandt J F ^a   Keating, David H ^a   Schwaegler, Tyler ^a   Schwalbach, Michael S ^a   Vinokur, Jeffrey ^a   Tremaine, Mary ^a   Peters, Jason M ^a,c   Kotlajich, Matthew V ^a   Pohlmann, Edward L ^a   Ong, Irene M ^a   Grass, Jeffrey A ^a   Kiley, Patricia J ^a,b   Landick, Robert ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; MESSENGER RNA; METHIONINE; RNA POLYMERASE;

ALCOHOL INTOXICATION; ALCOHOL TOLERANCE; ARTICLE; BACTERIAL STRAIN; BIOSYNTHESIS; CELL PROTECTION; CODON; DNA SEQUENCE; ESCHERICHIA COLI; GENE FREQUENCY; GENE MUTATION; GENOME; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REPRESSOR GENE; RIBOSOME; RNA CONFORMATION; RNA SEQUENCE; STRESS; TRANSCRIPTION TERMINATION;

ALLELES; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; ETHANOL; GENOME-WIDE ASSOCIATION STUDY; PROTEIN BIOSYNTHESIS; SOLVENTS; TRANSCRIPTION, GENETIC;

EID: 84903458015     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1401853111     Document Type: Article

References (83)

1. Yomano LP, York SW, Ingram LO (1998) Isolation and characterization of ethanoltolerant mutants of Escherichia coli KO11 for fuel ethanol production. J Ind Microbiol Biotechnol 20(2):132-138. (Pubitemid 28204301)
2. Dien BS, Cotta MA, Jeffries TW (2003) Bacteria engineered for fuel ethanol production: Current status. Appl Microbiol Biotechnol 63(3):258-266. (Pubitemid 38139281)
3. Zhao XQ, Bai FW (2009) Mechanisms of yeast stress tolerance and its manipulation for efficient fuel ethanol production. J Biotechnol 144(1):23-30.
4. Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314(5805):1565-1568. (Pubitemid 44907143)
5. Fischer CR, Klein-Marcuschamer D, Stephanopoulos G (2008) Selection and optimization of microbial hosts for biofuels production. Metab Eng 10(6):295-304.
6. Wackett LP (2008) Biomass to fuels via microbial transformations. Curr Opin Chem Biol 12(2):187-193.
7. Ingram LO (1990) Ethanol tolerance in bacteria. Crit Rev Biotechnol 9(4):305-319.
8. Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59(2):201- 222.
9. Segura A, et al. (2012) Solvent tolerance in Gram-negative bacteria. Curr Opin Biotechnol 23(3):415-421.
10. Dombek KM, Ingram LO (1984) Effects of ethanol on the Escherichia coli plasma membrane. J Bacteriol 157(1):233-239. (Pubitemid 14222481)
11. Ingram LO, Vreeland NS (1980) Differential effects of ethanol and hexanol on the Escherichia coli cell envelope. J Bacteriol 144(2):481-488. (Pubitemid 11164164)
12. Brynildsen MP, Liao JC (2009) An integrated network approach identifies the isobutanol response network of Escherichia coli. Mol Syst Biol 5:277.
13. Gonzalez R, et al. (2003) Gene array-based identification of changes that contribute to ethanol tolerance in ethanologenic Escherichia coli: Comparison of KO11 (parent) to LY01 (resistant mutant). Biotechnol Prog 19(2):612-623. (Pubitemid 36421015)
14. Freddolino PL, Goodarzi H, Tavazoie S (2012) Fitness landscape transformation through a single amino acid change in the Rho terminator. PLoS Genet 8(5):e1002744.
15. Goodarzi H, Hottes AK, Tavazoie S (2009) Global discovery of adaptive mutations. Nat Methods 6(8):581-583.
16. Nicolaou SA, Gaida SM, Papoutsakis ET (2012) Exploring the combinatorial genomic space in Escherichia coli for ethanol tolerance. Biotechnol J 7(11):1337-1345.
17. Woodruff LB, Boyle NR, Gill RT (2013) Engineering improved ethanol production in Escherichia coli with a genome-wide approach. Metab Eng 17:1-11.
18. Woodruff LB, et al. (2013) Genome-scale identification and characterization of ethanol tolerance genes in Escherichia coli. Metab Eng 15:124-133.
19. Zingaro KA, Papoutsakis ET (2012) Toward a semisynthetic stress response system to engineer microbial solvent tolerance. MBio 3(5):e00308-12.
20. Goodarzi H, et al. (2010) Regulatory and metabolic rewiring during laboratory evolution of ethanol tolerance in E. coli. Mol Syst Biol 6:378.
21. Chong H, et al. (2013) Improving ethanol tolerance of Escherichia coli by rewiring its global regulator cAMP receptor protein (CRP). PLoS ONE 8(2):e57628.
22. Alper H, Stephanopoulos G (2007) Global transcription machinery engineering: A new approach for improving cellular phenotype. Metab Eng 9(3):258-267. (Pubitemid 46809525)
23. Luo LH, et al. (2009) Improved ethanol tolerance in Escherichia coli by changing the cellular fatty acids composition through genetic manipulation. Biotechnol Lett 31(12): 1867-1871.
24. Friedman SM, Berezney R, Weinstein IB (1968) Fidelity in protein synthesis: The role of the ribosome. J Biol Chem 243(19):5044-5048.
25. Phoenix P, Melançon P, Brakier-Gingras L (1983) Characterization of mutants of Escherichia coli with an increased control of translation fidelity. Mol Gen Genet 189(1):123-128. (Pubitemid 13132887)
26. So AG, Davie EW (1964) The effects of organic solvents on protein biosynthesis and their influence on the amino acid code. Biochemistry 3:1165-1169.
27. VanBogelen RA, Kelley PM, Neidhardt FC (1987) Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J Bacteriol 169(1):26-32. (Pubitemid 17228684)
28. Potrykus K, Cashel M (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62:35-51.
29. Peters JM, Vangeloff AD, Landick R (2011) Bacterial transcription terminators: The RNA 3'-end chronicles. J Mol Biol 412(5):793-813.
30. Peters JM, et al. (2012) Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev 26(23):2621-2633.
31. Marincs F, Manfield IW, Stead JA, McDowall KJ, Stockley PG (2006) Transcript analysis reveals an extended regulon and the importance of protein-protein co-operativity for the Escherichia coli methionine repressor. Biochem J 396(2):227-234. (Pubitemid 43837238)
32. Bollen A, Cabezón T, de Wilde M, Villarroel R, Herzog A (1975) Alteration of ribosomal protein S17 by mutation linked to neamine resistance in Escherichia coli. I. General properties of neaA mutants. J Mol Biol 99(4):795-806.
33. Yaguchi M, et al. (1976) Alteration of ribosomal protein S17 by mutation linked to neamine resistance in Escherichia coli. II. Localization of the amino acid replacement in protein S17 from a neaA mutant. J Mol Biol 104(3):617-620.
34. Kramer EB, Farabaugh PJ (2007) The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 13(1):87-96. (Pubitemid 46026183)
35. Andrusiak K, Piotrowski JS, Boone C (2012) Chemical-genomic profiling: Systematic analysis of the cellular targets of bioactive molecules. Bioorg Med Chem 20(6):1952-1960.
36. Barker CA, Farha MA, Brown ED (2010) Chemical genomic approaches to study model microbes. Chem Biol 17(6):624-632.
37. Lando D, Cousin MA, Privat de Garilhe M (1973) Misreading, a fundamental aspect of the mechanism of action of several aminoglycosides. Biochemistry 12(22):4528-4533.
38. Demirci H, et al. (2013) A structural basis for streptomycin-induced misreading of the genetic code. Nat Commun 4:1355.
39. Gromadski KB, Rodnina MV (2004) Streptomycin interferes with conformational coupling between codon recognition and GTPase activation on the ribosome. Nat Struct Mol Biol 11(4):316-322. (Pubitemid 38436795)
40. Durfee T, et al. (2008) The complete genome sequence of Escherichia coli DH10B: Insights into the biology of a laboratory workhorse. J Bacteriol 190(7):2597-2606. (Pubitemid 351466356)
41. Momose H, Gorini L (1971) Genetic analysis of streptomycin dependence in Escherichia coli. Genetics 67(1):19-38.
42. Agarwal D, Gregory ST, O'Connor M (2011) Error-prone and error-restrictive mutations affecting ribosomal protein S12. J Mol Biol 410(1):1-9.
43. Zaher HS, Green R (2009) Quality control by the ribosome following peptide bond formation. Nature 457(7226):161-166.
44. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324(5924):218-223.
45. Peters JM, et al. (2009) Rho directs widespread termination of intragenic and stable RNA transcription. Proc Natl Acad Sci USA 106(36):15406-15411.
46. Bremer H, Dennis PP (1996) Modulation of chemical composition and other parameters of the cell by growth rate. Escherichia coli and Salmonella: Cellular and Molecular Biology, ed Neidhardt FC (American Society for Microbiology, Washington, DC), pp 1553-1569.
47. Nakamori S, Kobayashi S, Nishimura T, Takagi H (1999) Mechanism of L-methionine overproduction by Escherichia coli: The replacement of Ser-54 by Asn in the MetJ protein causes the derepression of L-methionine biosynthetic enzymes. Appl Microbiol Biotechnol 52(2):179-185. (Pubitemid 29424512)
48. Usuda Y, Kurahashi O (2005) Effects of deregulation of methionine biosynthesis on methionine excretion in Escherichia coli. Appl Environ Microbiol 71(6):3228-3234. (Pubitemid 40807234)
49. Flatley J, et al. (2005) Transcriptional responses of Escherichia coli to S-nitrosoglutathione under defined chemostat conditions reveal major changes in methionine biosynthesis. J Biol Chem 280(11):10065-10072. (Pubitemid 40395858)
50. Mordukhova EA, Lee HS, Pan JG (2008) Improved thermostability and acetic acid tolerance of Escherichia coli via directed evolution of homoserine o-succinyltransferase. Appl Environ Microbiol 74(24):7660-7668.
51. Gur E, Biran D, Gazit E, Ron EZ (2002) In vivo aggregation of a single enzyme limits growth of Escherichia coli at elevated temperatures. Mol Microbiol 46(5):1391-1397. (Pubitemid 36961272)
52. Record MT, Jr., Zhang W, Anderson CF (1998) Analysis of effects of salts and uncharged solutes on protein and nucleic acid equilibria and processes: A practical guide to recognizing and interpreting polyelectrolyte effects, Hofmeister effects, and osmotic effects of salts. Adv Protein Chem 51:281-353.
53. Chan CL, Landick R (1997) Effects of neutral salts on RNA chain elongation and pausing by Escherichia coli RNA polymerase. J Mol Biol 268(1):37-53. (Pubitemid 27192677)
54. Brandts JF, Hunt L (1967) The thermodynamics of protein denaturation. 3. The denaturation of ribonuclease in water and in aqueous urea and aqueous ethanol mixtures. J Am Chem Soc 89(19):4826-4838.
55. Bull HB, Breese K (1978) Interaction of alcohols with proteins. Biopolymers 17(9):2121-2131. (Pubitemid 9015224)
56. Lehmann MS, Mason SA, McIntyre GJ (1985) Study of ethanol-lysozyme interactions using neutron diffraction. Biochemistry 24(21):5862-5869. (Pubitemid 16203026)
57. 32. Nature 329(6137):348-351. (Pubitemid 17134361)
58. Giudice E, Gillet R (2013) The task force that rescues stalled ribosomes in bacteria. Trends Biochem Sci 38(8):403-411.
59. Jerinic O, Joseph S (2000) Conformational changes in the ribosome induced by translational miscoding agents. J Mol Biol 304(5):707-713. (Pubitemid 32047075)
60. Baldridge KC, Contreras LM (2014) Functional implications of ribosomal RNA methylation in response to environmental stress. Crit Rev Biochem Mol Biol 49(1):69-89.
61. Urbonavičius J, Durand JM, Björk GR (2002) Three modifications in the D and T arms of tRNA influence translation in Escherichia coli and expression of virulence genes in Shigella flexneri. J Bacteriol 184(19):5348-5357.
62. Gorini L, Rosset R, Zimmermann RA (1967) Phenotype masking and streptomycin dependence. Science 157(3794):1314-1317.
63. Klein-Marcuschamer D, Santos CN, Yu H, Stephanopoulos G (2009) Mutagenesis of the bacterial RNA polymerase alpha subunit for improvement of complex phenotypes. Appl Environ Microbiol 75(9):2705-2711.
64. Kanjee U, Ogata K, Houry WA (2012) Direct binding targets of the stringent response alarmone (p)ppGpp. Mol Microbiol 85(6):1029-1043.
65. Heath RJ, Jackowski S, Rock CO (1994) Guanosine tetraphosphate inhibition of fatty acid and phospholipid synthesis in Escherichia coli is relieved by overexpression of glycerol-3-phosphate acyltransferase (plsB). J Biol Chem 269(42):26584-26590.
66. Merlie JP, Pizer LI (1973) Regulation of phospholipid synthesis in Escherichia coli by guanosine tetraphosphate. J Bacteriol 116(1):355-366.
67. Cronan JE, Jr., Weisberg LJ, Allen RG (1975) Regulation of membrane lipid synthesis in Escherichia coli: Accumulation of free fatty acids of abnormal length during inhibition of phospholipid synthesis. J Biol Chem 250(15):5835-5840.
68. Dalebroux ZD, Swanson MS (2012) ppGpp: Magic beyond RNA polymerase. Nat Rev Microbiol 10(3):203-212.
69. - mutations in yeast Saccharomyces cerevisiae by ethanol. Mutat Res 71(2):193-199. (Pubitemid 10066798)
70. Miller JH (1972) Experiments in Molecular Genetics (Cold Spring Harbor Laboratory Press, Plainview, NY).
71. Baba T, et al. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2:2006.0008.
72. Das A, Court D, Adhya S (1976) Isolation and characterization of conditional lethal mutants of Escherichia coli defective in transcription termination factor rho. Proc Natl Acad Sci USA 73(6):1959-1963.
73. Schwalbach MS, et al. (2012) Complex physiology and compound stress responses during fermentation of alkali-pretreated corn stover hydrolysate by an Escherichia coli ethanologen. Appl Environ Microbiol 78(9):3442-3457.
74. Artsimovitch I, Landick R (2002) The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109(2):193-203. (Pubitemid 34518258)
75. Gribskov M, Burgess RR (1983) Overexpression and purification of the sigma subunit of Escherichia coli RNA polymerase. Gene 26(2-3):109-118. (Pubitemid 14190463)
76. Toulokhonov I, Zhang J, Palangat M, Landick R (2007) A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing. Mol Cell 27(3):406-419. (Pubitemid 47126936)
77. Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119(3):736-747.
78. Sasson V, Shachrai I, Bren A, Dekel E, Alon U (2012) Mode of regulation and the insulation of bacterial gene expression. Mol Cell 46(4):399-407.
79. Zaslaver A, et al. (2006) A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Methods 3(8):623-628. (Pubitemid 44123429)
80. Oh E, et al. (2011) Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 147(6):1295-1308.
81. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754-1760.
82. O'Connor PB, Li GW, Weissman JS, Atkins JF, Baranov PV (2013) rRNA:mRNA pairing alters the length and the symmetry of mRNA-protected fragments in ribosome profiling experiments. Bioinformatics 29(12):1488-1491.
83. Blattner FR, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277(5331):1453-1462. (Pubitemid 27449228)