Changes in gene expression of E. coli under conditions of modeled reduced gravity

Microgravity Science and Technology

Volumn 20, Issue 1, 2008, Pages 41-57

  Vukanti, Raja ^a   Mintz, Eric ^a   Leff, Laura ^a  

^a KENT STATE UNIVERSITY   (United States)

Author keywords

Bacteria; Clinorotation; Gene expression; Microarray; Microgravity

Indexed keywords

BACTERIA; GENE EXPRESSION; MICROARRAYS; MICROGRAVITY;

CLINOROTATION; STARVATION RESPONSE;

ESCHERICHIA COLI;

EID: 44449129109     PISSN: 09380108     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12217-008-9012-9     Document Type: Article

References (75)

1. Ackerley, D.F., Barak, Y., Lynch, S.V., Curtin, J., Matin, A.: Effect of chromate stress on Escherichia coli K-12. J. Bacteriol. 188, 3371 (2006)
2. Albrecht-Buehler, G.: Possible mechanisms of indirect gravity sensing by cells. Gravit. Space Biol. Bull. 4, 25 (1991)
3. Baker, P.W., Leff, L.G.: The effect of simulated microgravity on bacteria from the Mir space station. Microgravity Sci. Technol. 15, 35 (2004)
4. Baker, P.W., Leff, L.G.: Attachment to stainless steel by Mir Space Station bacteria growing under modeled reduced gravity at varying nutrient concentrations. Biofilms 2, 1 (2005a)
5. Baker, P.W., Leff, L.G.: Intraspecific differences in bacterial responses to modelled reduced gravity. J. Appl. Microbiol. 98, 1239 (2005b)
6. Baker, P.W., Leff, L.G.: Mir space station bacteria responses to modeled reduced gravity under starvation conditions. Adv. Space Res. 38, 1152 (2006)
7. Baker, P.W., Meyer, M.L., Leff, L.G.: Escherichia coli growth under modeled reduced gravity. Microgravity Sci. Technol. 15, 39 (2004)
8. Beloin, C., Valle, J., Latour-Lambert, P., Faure, P., Kzreminski, M., Balestrino, D., Haagensen, J.A., Molin, S., Prensier, G., Arbeille, B., Ghigo, J.M.: Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Microbiol. 51, 659 (2004)
9. Benjamini, Y., Hochberg, Y.: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Stat. Methodol. 57, 289 (1995)
10. Bishop, R.E., Leskiw, B.K., Hodges, R.S., Kay, C.M., Weiner, J.H.: The entericidin locus of Escherichia coli and its implications for programmed bacterial cell death. J. Mol. Biol. 280, 583 (1998)
11. Boos, W., Ehmann, U., Bremer, E., Middendorf, A., Postma, P.: Trehalase of Escherichia coli. Mapping and cloning of its structural gene and identification of the enzyme as a periplasmic protein induced under high osmolarity growth conditions. J. Biol. Chem. 262, 13212 (1987)
12. Boot, I.R., Cash, P., O'Byrne, C.: Sensing and adapting to acid stress. Antonie Van Leeuwenhoek 81, 33 (2002)
13. Brown, R.B., Klaus, D., Todd, P.: Effects of space flight, clinorotation, and centrifugation on the substrate utilization efficiency of E. coli. Microgravity Sci. Technol. 13, 24 (2002)
14. Cashel, M., Gentry, D.R., Hernandez, V.J., Vinella, D.: The stringent response. In: Neidhardt, F.C., Curtiss III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., Reznikoff, W.S, Riley, M., Schaechter, M., Umbarger, H.E. (eds.) Escherichia coli and Salmonella: cellular and molecular biology, p. 1458. ASM, Washington, D.C. (1996)
15. Chang, L., Wei, L.I., Audia, J.P., Morton, R.A., Schellhorn, H.E.: Expression of the Escherichia coli NRZ nitrate reductase is highly growth phase dependent and is controlled by RpoS, the alternative vegetative sigma factor. Mol. Microbiol. 34, 756 (1999)
16. Checroun, C., Gutierrez, C.: Sigma(s)-dependent regulation of yehZYXW, which encodes a putative osmoprotectant ABC transporter of Escherichia coli. FEMS Microbiol. Lett. 236, 221 (2004)
17. Death, A., Ferenci, T.: The importance of the binding-protein-dependent Mgl system to the transport of glucose in Escherichia coli growing on low sugar concentrations. Res-Microbiol. 144, 529 (1993)
18. Elledge, S.J., Walker, G.C.: Proteins required for ultraviolet light and chemical mutagenesis. Identification of the products of the umuC locus of Escherichia coli. J. Mol. Biol. 164, 175 (1983)
19. England, L.S., Gorzelak, M., Trevors, J.T.: Growth and membrane polarization in Pseudomonas aeruginosa UG2 grown in randomized microgravity in a high aspect ratio vessel. Biochim. Biophys. Acta 1624, 76 (2003)
20. Ferrandez, A., Minambres, B., Garcia, B., Olivera, E.R., Luengo, J.M., Garcia, J.L., Diaz, E.: Catabolism of phenylacetic acid in Escherichia coli. Characterization of a new aerobic hybrid pathway. J. Biol. Chem. 273, 25974 (1998)
21. Gao, H., Ayyaswamy, P.S., Ducheyne, P.: Dynamics of a microcarrier particle in the simulated microgravity environment of a rotating-wall vessel. Microgravity Sci. Technol. 10, 154 (1997)
22. Gao, Q., Fang, A., Pierson, D.L., Mishra, S.K., Demain, A.L.: Shear stress enhances microcin B17 production in a rotating wall bioreactor, but ethanol stress does not. Appl. Microbiol. Biotechnol. 56, 384 (2001)
23. Gimenez, R., Nunez, M.F., Badia, J., Aguilar, J., Baldoma, L.: The gene yjcG, cotranscribed with the gene acs, encodes an acetate permease in Escherichia coli. J. Bacteriol. 185, 6448 (2003)
24. Hammond, T.G., Hammond, J.M.: Optimized suspension culture: the rotating-wall vessel. Am. J. Physiol. Renal. Physiol. 281, F12 (2001)
25. Harder, W., Dijkhuizen, L.: Physiological Responses to Nutrient Limitation. Annu. Rev. Microbiol. 37, 1 (1983)
26. Helling, R.B.: Why does Escherichia coli have two primary pathways for synthesis of glutamate? J. Bacteriol. 176, 4664 (1994)
27. Hengge-Aronis, R.: Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66, 373 (2002)
28. Hood, M.A., Guckert, J.B., White, D.C., Deck, F.: Effect of nutrient deprivation on lipid, carbohydrate, DNA, RNA, and protein levels in Vibrio cholerae. Appl Environ Microbiol. 52, 788 (1986)
29. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., Speed, T.P.: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249 (2003)
30. Kacena, M.A., Manfredi, B., Todd, P.: Effects of space flight and mixing on bacterial growth in low volume cultures. Microgravity Sci. Technol. 12, 74 (1999a)
31. Kacena, M.A., Merrell, G.A., Manfredi, B., Smith, E.E., Klaus, D.M., Todd, P.: Bacterial growth in space flight: logistic growth curve parameters for Escherichia coli and Bacillus subtilis. Appl. Microbiol. Biotechnol. 51, 229 (1999b)
32. Keseler, I.M., Collado-Vides, J., Gama-Castro, S., Ingraham, J., Paley, S., Paulsen, I.T., Peralta-Gil, M., Karp, P.D.: EcoCyc: a comprehensive database resource for Escherichia coli. Nucl. Acids Res. 33, D334 (2005)
33. Klaus, D.M.: Clinostats and bioreactors. Gravit. Space Biol. Bull. 14, 55 (2001)
34. Klaus, D., Simske, S., Todd, P., Stodieck, L.: Investigation of space flight effects on Escherichia coli and a proposed model of underlying physical mechanisms. Microbiology 143, 449 (1997)
35. Klaus, D.M., Todd, P., Schatz, A.: Functional weightlessness during clinorotation of cell suspensions. Adv. Space Res. 21, 1315 (1998)
36. Kovárová-Kovar, K., Egli, T.: Growth kinetics of suspended microbial cells: from single-substrate-controlled growth to mixed-substrate kinetics. Microbiol. Mol. Bio. Rev. 62, 646 (1998)
37. Lessard, I.A., Pratt, S.D., McCafferty, D.G., Bussiere, D.E., Hutchins, C., Wanner, B.L., Katz, L., Walsh, C.T.: Homologs of the vancomycin resistance D-Ala-D-Ala dipeptidase VanX in Streptomyces toyocaensis, Escherichia coli and Synechocystis: attributes of catalytic efficiency, stereoselectivity and regulation with implications for function. Chemistry 5, 489 (1998)
38. Leyh, T.S., Taylor, J.C., Markham, G.D.: The sulfate activation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization. J. Biol. Chem. 263, 2409 (1988)
39. Liu, X., Ferenci, T.: Regulation of Porin-Mediated Outer Membrane Permeability by Nutrient Limitation in Escherichia coli. J. Bacteriol. 180, 3917 (1998)
40. Loewen, P.: Probing the structure of catalase HPII of Escherichia coli. Gene 179, 39 (1996)
41. Lynch, S.V., Brodie, E.L., Matin, A.: Role and regulation of sigma S in general resistance conferred by low-shear simulated microgravity in Escherichia coli. J. Bacteriol. 186, 8207 (2004)
42. Ma, Z., Richard, H., Tucker, D.L., Conway, T., Foster, J.W.: Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J. Bacteriol. 184, 7001 (2002)
43. Mårdén, P., Tunlid, A., Malmcrona-Friberg, K., Odham, G., Kjelleberg, S.: Physiological and morphological changes during short term starvation of marine bacterial islates. Arch. Microbiol. 142, 326 (1985)
44. Marschall, C., Labrousse, V., Kreimer, M., Weichart, D., Kolb, A., Hengge-Aronis, R.: Molecular analysis of the regulation of csiD, a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on sigma s and requires activation by cAMP-CRP. J. Mol. Biol. 276, 339 (1998)
45. Masse, E., Gottesman, S.: A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 99, 4620 (2002)
46. McLean, R.J., Cassanto, J.M., Barnes, M.B., Koo, J.H.: Bacterial biofilm formation under microgravity conditions. FEMS Microbiol. Lett. 195, 115 (2001)
47. McPherson, A.: Effects of a microgravity environment on the crystallization of biological macromolecules. Microgravity Sci. Technol. VI, 101 (1993)
48. Mendez-Ortiz, M.M., Hyodo, M., Hayakawa, Y., Membrillo-Hernandez, J.: Genome-wide transcriptional profile of Escherichia coli in response to high levels of the second messenger 3ô,5ô-cyclic diguanylic acid. J. Biol. Chem. 281, 8090 (2006)
49. Mennigmann, H.D., Lange, M.: Growth and differentiation of Bacillus subtilis under microgravity. Naturwissenschaften 73, 415 (1986)
50. Metzner, M., Germer, J., Hengge, R.: Multiple stress signal integration in the regulation of the complex sigma S-dependent csiD-ygaF-gabDTP operon in Escherichia coli. Mol. Microbiol. 51, 799 (2004)
51. Mey, A.R., Craig, S.A., Payne, S.M.: Characterization of Vibrio cholerae RyhB: the RyhB Regulon and Role of ryhB in Biofilm Formation. Infect. Immun. 73, 5706 (2005)
52. Nickerson, C.A., Ott, C.M.: Three dimensional cell culture models for infectious disease and drug development. Bioforum Eur. 1-2, 22 (2006)
53. Nickerson, C.A., Ott, C.M., Mister, S.J., Morrow, B.J., Burns-Keliher, L., Pierson, D.L.: Microgravity as a Novel Environmental Signal Affecting Salmonella enterica Serovar Typhimurium Virulence. Infect. Immun. 68, 3147 (2000)
54. Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R., LeBlanc, C.L., Honer zu Bentrup, K., Hammond, T., Pierson, D.L.: Low-shear modeled microgravity: a global environmental regulatory signal affecting bacterial gene expression, physiology, and pathogenesis. J. Microbiol. Methods 54, 1 (2003)
55. Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R., Pierson, D.L.: Microbial responses to microgravity and other low-shear environments. Microbiol. Mol. Biol. Rev. 68, 345 (2004)
56. Osborne, M.J., Siddiqui, N., Iannuzzi, P., Gehring, K.: The solution structure of ChaB, a putative membrane ion antiporter regulator from Escherichia coli. BMC Struct. Biol. 4, 9 (2004) DOI 10.1186/1472-6807-4-9.
57. Pfaffl, M.W.: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001)
58. Pomposiello, P.J., Demple, B.: Global adjustment of microbial physiology during free radical stress. Adv. Microb. Physiol. 46, 319 (2002)
59. Quadroni, M., Staudenmann, W., Kertesz, M., James, P.: Analysis of global responses by protein and peptide fingerprinting of proteins isolated by two-dimensional gel electrophoresis. Application to the sulfate-starvation response of Escherichia coli. Eur. J. Biochem. 239, 773 (1996)
60. Salgado, H., Gama-Castro, S., Martinez-Antonio, A., Diaz-Peredo, E., Sanchez-Solano, F., Peralta-Gil, M., Garcia-Alonso, D., Jimenez-Jacinto, V., Santos-Zavaleta, A., Bonavides-Martinez, C., Collado-Vides, J.: RegulonDB (version 4.0): transcriptional regulation, operon organization and growth conditions in Escherichia coli K-12. Nucleic Acids Res. 32, D303 (2004)
61. Seputiene, V., Motiejunas, D., Suziedelis, K., Tomenius, H., Normark, S., Melefors, O., Suziedeliene, E.: Molecular characterization of the acid-inducible asr gene of Escherichia coli and its role in acid stress response. J. Bacteriol. 185, 2475 (2003)
62. Shin, S., Song, S.G., Lee, D.S., Pan, J.G., Park, C.: Involvement of iclR and rpoS in the induction of acs, the gene for acetyl coenzyme A synthetase of Escherichia coli K-12. FEMS Microbiol. Lett. 146, 103 (1997)
63. Siegel, L.M., Murphy, M.J., Kamin, H.: Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of enterobacteria. I. The Escherichia coli hemoflavoprotein: molecular parameters and prosthetic groups. J. Biol. Chem. 248, 251 (1973)
64. Sirko, A., Hryniewicz, M., Hulanicka, D., Bock, A.: Sulfate and thiosulfate transport in Escherichia coli K-12: nucleotide sequence and expression of the cysTWAM gene cluster. J. Bacteriol. 172, 3351 (1990)
65. Suziedeliene, E., Suziedelis, K., Garbenciute, V., Normark, S.: The acid-inducible asr gene in Escherichia coli: transcriptional control by the phoBR operon. J. Bacteriol. 181, 2084 (1999)
66. Tempest, D.W., Neijssel, O.M., Zevenboom, W.: Properties and performances in laboratory cultures; their relevance to growth in natural ecosystems. Symp. Soc. Gen. Microbiol. 34, 119 (1983)
67. Thevenet, D., D'Ari, R., Bouloc, P.: The SIGNAL experiment in BIORACK: Escherichia coli in microgravity. J. Biotechnol. 47, 89 (1996)
68. Tucker, D.L., Ott, C.M., Huff, S., Fofanov, Y., Pierson, D.L., Willson, R.C., Fox, G.E.: Characterization of Escherichia coli MG1655 grown in a low-shear modeled microgravity environment. BMC Microbiol. 7, 15 (2007) DOI 10.1186/1471-2180-7-15.
69. Wilson, J.W., Ott, C.M., Ramamurthy, R., Porwollik, S., McClelland, M., Pierson, D.L., Nickerson, C.A.: Low-Shear modeled microgravity alters the Salmonella enterica serovar typhimurium stress response in an RpoS-independent manner. Appl. Environ. Microbiol. 68, 5408 (2002a)
70. Wilson, J.W., Ramamurthy, R., Porwollik, S., McClelland, M., Hammond, T., Allen, P., Ott, C.M., Pierson, D.L., Nickerson, C.A.: Microarray analysis identifies Salmonella genes belonging to the low-shear modeled microgravity regulon. Proc. Natl. Acad. Sci. U. S. A. 99, 13807 (2002b)
71. Xi, H., Schneider, B.L., Reitzer, L.: Purine catabolism in Escherichia coli and function of xanthine dehydrogenase in purine salvage. J. Bacteriol. 182, 5332 (2000)
72. Xu, J., Johnson, R.C.: aldB, an RpoS-dependent gene in Escherichia coli encoding an aldehyde dehydrogenase that is repressed by Fis and activated by Crp. J. Bacteriol. 177, 3166 (1995)
73. Yamada, M., Talukder, A.A., Nitta, T.: Characterization of the ssnA gene, which is involved in the decline of cell viability at the beginning of stationary phase in Escherichia coli. J. Bacteriol. 181, 1838 (1999)
74. Yamanaka, K., Inouye, M.: Growth-phase-dependent expression of cspD, encoding a member of the CspA family in Escherichia coli. J. Bacteriol. 179, 5 126 (1997)
75. Zimmer, D.P., Soupene, E., Lee, H.L., Wendisch, V.F., Khodursky, A.B., Peter, B.J., Bender, R.A., Kustu, S.: Nitrogen regulatory protein C-controlled genes of Escherichia coli: Scavenging as a defense against nitrogen limitation. Proc. Natl. Acad. Sci. U. S. A. 97, 14674 (2000)