Home LiteratureArticle Details
PMID: 11395452 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate.

Journal of bacteriology ·Vol. 183 ·No. 13 ·2001-07-00 ·Pages 3890-902

Pomposiello PJ, Bennik MH, Demple B

Abstract

Escherichia coli responds to oxidative stress by activating sets of coregulated genes that help the cell to maintain homeostasis. Identified previously by genetic and biochemical approaches, the soxRS system mediates the induction of 18 of these redox-inducible genes (including the soxS gene itself). An overlapping set of genes is activated by an assortment of structurally unrelated molecules with antibiotic activities; many genes in this response are controlled by the marRAB system. The activation of either the soxRS or the marRAB system results in enhanced resistance to both superoxide-generating agents and multiple antibiotics. In order to probe the extent of these regulatory networks, we have measured whole-genome transcriptional profiles of the E. coli response to the superoxide-generating agent paraquat (PQ), an inducer of the soxRS system, and to the weak acid salt sodium salicylate (NaSal), an inducer of the marRA system. A total of 112 genes was modulated in response to PQ, while 134 genes were modulated in response to NaSal. We have also obtained transcriptional profiles of the SoxS and MarA regulons in the absence of global stress, in order to establish the regulatory hierarchies within the global responses. Several previously unrelated genes were shown to be under SoxS or MarA control. The genetic responses to both environmental insults revealed several common themes, including the activation of genes coding for functions that replenish reducing potential; regulate iron transport and storage; and participate in sugar and amino acid transport, detoxification, protein modification, osmotic protection, and peptidoglycan synthesis. A large number of PQ- and NaSal-responsive genes have no known function, suggesting that many adaptive metabolic changes that ensue after stress remain uncharacterized.

MeSH Terms
Bacterial Proteins/metabolism Blotting, Northern DNA-Binding Proteins/metabolism Environment Escherichia coli/drug effects,genetics Escherichia coli Proteins Gene Expression Profiling/methods Gene Expression Regulation, Bacterial Genome, Bacterial Oxidative Stress/genetics Paraquat/pharmacology Sodium Salicylate/pharmacology Superoxides/pharmacology Trans-Activators Transcription Factors/metabolism Transcription, Genetic
Chemicals
Bacterial Proteins DNA-Binding Proteins Escherichia coli Proteins MarA protein, E coli Trans-Activators Transcription Factors Superoxides SoxS protein, E coli Paraquat Sodium Salicylate
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Pomposiello P J
Department of Cancer Cell Biology, Harvard School of Public Health, Boston, Massachusetts 02115, USA.
Bennik M H
Demple B
References (46)
46 references, click to expand
  1. The transcriptional profile of early to middle sporulation in Bacillus subtilis.
    Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):8063-8 PMID: 10869437
  2. Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA.
    J Bacteriol. 2000 Jun;182(12):3467-74 PMID: 10852879
  3. Global gene expression profiling in Escherichia coli K12. The effects of integration host factor.
    J Biol Chem. 2000 Sep 22;275(38):29672-84 PMID: 10871608
  4. Genomic expression programs in the response of yeast cells to environmental changes.
    Mol Biol Cell. 2000 Dec;11(12):4241-57 PMID: 11102521
  5. Global analysis of the genetic network controlling a bacterial cell cycle.
    Science. 2000 Dec 15;290(5499):2144-8 PMID: 11118148
  6. Redox-operated genetic switches: the SoxR and OxyR transcription factors.
    Trends Biotechnol. 2001 Mar;19(3):109-14 PMID: 11179804
  7. Biochemical characterization of a paraquat-tolerant mutant of Escherichia coli.
    J Biol Chem. 1985 Sep 5;260(19):10478-81 PMID: 3897218
  8. Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):8917-21 PMID: 3321061
  9. marA locus causes decreased expression of OmpF porin in multiple-antibiotic-resistant (Mar) mutants of Escherichia coli.
    J Bacteriol. 1988 Dec;170(12):5416-22 PMID: 2848006
  10. A global response induced in Escherichia coli by redox-cycling agents overlaps with that induced by peroxide stress.
    J Bacteriol. 1989 Jul;171(7):3933-9 PMID: 2472381
  11. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation.
    Science. 1990 Apr 13;248(4952):189-94 PMID: 2183352
  12. soxR, a locus governing a superoxide response regulon in Escherichia coli K-12.
    J Bacteriol. 1990 Aug;172(8):4197-205 PMID: 1695893
  13. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli.
    Proc Natl Acad Sci U S A. 1990 Aug;87(16):6181-5 PMID: 1696718
  14. Activation of oxidative stress genes by mutations at the soxQ/cfxB/marA locus of Escherichia coli.
    J Bacteriol. 1991 Jul;173(14):4433-9 PMID: 1648558
  15. Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon.
    Nucleic Acids Res. 1991 Aug 25;19(16):4479-84 PMID: 1653416
  16. Disruption of the gene for Met-tRNA(fMet) formyltransferase severely impairs growth of Escherichia coli.
    J Bacteriol. 1992 Jul;174(13):4294-301 PMID: 1624424
  17. Posttranscriptional repression of Escherichia coli OmpF protein in response to redox stress: positive control of the micF antisense RNA by the soxRS locus.
    J Bacteriol. 1993 Feb;175(4):1026-31 PMID: 7679383
  18. Negative autoregulation by the Escherichia coli SoxS protein: a dampening mechanism for the soxRS redox stress response.
    J Bacteriol. 1993 Nov;175(22):7492-4 PMID: 8226698
  19. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid.
    Science. 1993 Dec 17;262(5141):1883-6 PMID: 8266079
  20. NADPH: ferredoxin oxidoreductase acts as a paraquat diaphorase and is a member of the soxRS regulon.
    Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1328-31 PMID: 8108411
  21. Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli.
    J Bacteriol. 1995 Jun;177(12):3414-9 PMID: 7768850
  22. Binding of purified multiple antibiotic-resistance repressor protein (MarR) to mar operator sequences.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5456-60 PMID: 7777530
  23. Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli.
    Mol Microbiol. 1995 Apr;16(1):45-55 PMID: 7651136
  24. Autoactivation of the marRAB multiple antibiotic resistance operon by the MarA transcriptional activator in Escherichia coli.
    J Bacteriol. 1996 Apr;178(8):2216-23 PMID: 8636021
  25. Identification for mar mutants among quinolone-resistant clinical isolates of Escherichia coli.
    Antimicrob Agents Chemother. 1996 Jul;40(7):1695-8 PMID: 8807064
  26. SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form.
    Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10094-8 PMID: 8816757
  27. Overlaps and parallels in the regulation of intrinsic multiple-antibiotic resistance in Escherichia coli.
    Mol Microbiol. 1996 Aug;21(3):441-8 PMID: 8866468
  28. The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor.
    J Biol Chem. 1996 Dec 27;271(52):33173-5 PMID: 8969171
  29. Paraquat regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12 is SoxRS independent but modulated by sigma S.
    J Bacteriol. 1997 May;179(10):3164-70 PMID: 9150210
  30. The complete genome sequence of Escherichia coli K-12.
    Science. 1997 Sep 5;277(5331):1453-62 PMID: 9278503
  31. Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon.
    Antimicrob Agents Chemother. 1997 Oct;41(10):2067-75 PMID: 9333027
  32. Genes and proteins of Escherichia coli K-12.
    Nucleic Acids Res. 1998 Jan 1;26(1):54 PMID: 9399799
  33. The H2O2 stimulon in Saccharomyces cerevisiae.
    J Biol Chem. 1998 Aug 28;273(35):22480-9 PMID: 9712873
  34. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein.
    EMBO J. 1998 Oct 15;17(20):6061-8 PMID: 9774349
  35. Global response of Saccharomyces cerevisiae to an alkylating agent.
    Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1486-91 PMID: 9990050
  36. Small RNAs in Escherichia coli.
    Trends Microbiol. 1999 Jan;7(1):37-45 PMID: 10068996
  37. OxyR and SoxRS regulation of fur.
    J Bacteriol. 1999 Aug;181(15):4639-43 PMID: 10419964
  38. Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro.
    J Bacteriol. 1999 Aug;181(15):4669-72 PMID: 10419969
  39. Genome-wide expression profiling in Escherichia coli K-12.
    Nucleic Acids Res. 1999 Oct 1;27(19):3821-35 PMID: 10481021
  40. Functional genomics: expression analysis of Escherichia coli growing on minimal and rich media.
    J Bacteriol. 1999 Oct;181(20):6425-40 PMID: 10515934
  41. Structural requirements for marbox function in transcriptional activation of mar/sox/rob regulon promoters in Escherichia coli: sequence, orientation and spatial relationship to the core promoter.
    Mol Microbiol. 1999 Nov;34(3):431-41 PMID: 10564485
  42. Identification of SoxS-regulated genes in Salmonella enterica serovar typhimurium.
    J Bacteriol. 2000 Jan;182(1):23-9 PMID: 10613858
  43. Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5146-50 PMID: 10805777
  44. Defining a rob regulon in Escherichia coli by using transposon mutagenesis.
    J Bacteriol. 2000 Jul;182(13):3794-801 PMID: 10850996
  45. Fur positive regulation of iron superoxide dismutase in Escherichia coli: functional analysis of the sodB promoter.
    J Bacteriol. 2000 Jul;182(13):3802-8 PMID: 10850997
  46. 6S RNA regulates E. coli RNA polymerase activity.
    Cell. 2000 Jun 9;101(6):613-23 PMID: 10892648
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2001-07-00
Pages
3890-902
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC95271
Subset
IM
Grants
NCI NIH HHS · R01 CA037831 · United States
NCI NIH HHS · CA37831 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com