Home LiteratureArticle Details
PMID: 22406834 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Extracting regulator activity profiles by integration of de novo motifs and expression data: characterizing key regulators of nutrient depletion responses in Streptomyces coelicolor.

Nucleic acids research ·Vol. 40 ·No. 12 ·2012-07-00 ·Pages 5227-39

Iqbal M, Mast Y, Amin R, Hodgson DA, STREAM Consortium, Wohlleben W, Burroughs NJ

Abstract

Determining transcriptional regulator activities is a major focus of systems biology, providing key insight into regulatory mechanisms and co-regulators. For organisms such as Escherichia coli, transcriptional regulator binding site data can be integrated with expression data to infer transcriptional regulator activities. However, for most organisms there is only sparse data on their transcriptional regulators, while their associated binding motifs are largely unknown. Here, we address the challenge of inferring activities of unknown regulators by generating de novo (binding) motifs and integrating with expression data. We identify a number of key regulators active in the metabolic switch, including PhoP with its associated directed repeat PHO box, candidate motifs for two SARPs, a CRP family regulator, an iron response regulator and that for LexA. Experimental validation for some of our predictions was obtained using gel-shift assays. Our analysis is applicable to any organism for which there is a reasonable amount of complementary expression data and for which motifs (either over represented or evolutionary conserved) can be identified in the genome.

MeSH Terms
Bacterial Proteins/metabolism Binding Sites Gene Expression Profiling Gene Regulatory Networks Genomics/methods Glutamic Acid/metabolism Nucleotide Motifs Phosphates/metabolism Streptomyces coelicolor/genetics,metabolism Transcription Factors/metabolism Transcriptome
Chemicals
Bacterial Proteins Phosphates Transcription Factors PhoP protein, Bacteria Glutamic Acid
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Iqbal Mudassar
Multidisciplinary Centre for Integrative Biology (MyCIB), School of Biosciences, University of Nottingham, Nottingham, UK. mudassar.iqbal@nottingham.ac.uk
Mast Yvonne
Amin Rafat
Hodgson David A
STREAM Consortium
Wohlleben Wolfgang
Burroughs Nigel J
References (48)
48 references, click to expand
  1. A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils.
    Genes Dev. 2003 Jul 15;17(14):1714-26 PMID: 12832396
  2. Factor analysis for gene regulatory networks and transcription factor activity profiles.
    BMC Bioinformatics. 2007 Feb 23;8:61 PMID: 17319944
  3. The dynamic architecture of the metabolic switch in Streptomyces coelicolor.
    BMC Genomics. 2010 Jan 06;11:10 PMID: 20053288
  4. Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877.
    Microbiology (Reading). 2006 Nov;152(Pt 11):3355-3366 PMID: 17074905
  5. Phosphate control over nitrogen metabolism in Streptomyces coelicolor: direct and indirect negative control of glnR, glnA, glnII and amtB expression by the response regulator PhoP.
    Nucleic Acids Res. 2009 Jun;37(10):3230-42 PMID: 19321498
  6. Formation and reversion of Streptomycete protoplasts: cultural condition and morphological study.
    J Gen Microbiol. 1974 Feb;80(2):389-400 PMID: 4207870
  7. Defining transcriptional networks through integrative modeling of mRNA expression and transcription factor binding data.
    BMC Bioinformatics. 2004 Mar 18;5:31 PMID: 15113405
  8. The zinc-responsive regulator Zur and its control of the znu gene cluster encoding the ZnuABC zinc uptake system in Escherichia coli.
    J Biol Chem. 2000 Aug 11;275(32):24321-32 PMID: 10816566
  9. Genome-wide transcriptome analysis reveals that a pleiotropic antibiotic regulator, AfsS, modulates nutritional stress response in Streptomyces coelicolor A3(2).
    BMC Genomics. 2008 Jan 29;9:56 PMID: 18230178
  10. Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs.
    FEMS Microbiol Rev. 2003 Dec;27(5):559-92 PMID: 14638413
  11. Phosphinothricin-tripeptide biosynthesis: an original version of bacterial secondary metabolism?
    Phytochemistry. 2009 Oct-Nov;70(15-16):1787-800 PMID: 19878959
  12. Regulation of the furA and catC operon, encoding a ferric uptake regulator homologue and catalase-peroxidase, respectively, in Streptomyces coelicolor A3(2).
    J Bacteriol. 2000 Jul;182(13):3767-74 PMID: 10850993
  13. Bayesian sparse hidden components analysis for transcription regulation networks.
    Bioinformatics. 2006 Mar 15;22(6):739-46 PMID: 16368767
  14. Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a DeltaphoP mutant.
    Proteomics. 2007 Jul;7(14):2410-29 PMID: 17623301
  15. Model-based method for transcription factor target identification with limited data.
    Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):7793-8 PMID: 20385836
  16. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces.
    EMBO Rep. 2008 Jul;9(7):670-5 PMID: 18511939
  17. A comprehensive library of DNA-binding site matrices for 55 proteins applied to the complete Escherichia coli K-12 genome.
    J Mol Biol. 1998 Nov 27;284(2):241-54 PMID: 9813115
  18. A novel family of proteins that regulates antibiotic production in streptomycetes appears to contain an OmpR-like DNA-binding fold.
    Mol Microbiol. 1997 Sep;25(6):1181-4 PMID: 9350875
  19. Bioinformatic identification of novel regulatory DNA sequence motifs in Streptomyces coelicolor.
    BMC Microbiol. 2004 Apr 08;4:14 PMID: 15072583
  20. sigmaR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2).
    EMBO J. 1998 Oct 1;17(19):5776-82 PMID: 9755177
  21. i-Tracker: for quantitative proteomics using iTRAQ.
    BMC Genomics. 2005 Oct 20;6:145 PMID: 16242023
  22. BATS: a Bayesian user-friendly software for analyzing time series microarray experiments.
    BMC Bioinformatics. 2008 Oct 06;9:415 PMID: 18837969
  23. Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation.
    J Mol Microbiol Biotechnol. 2007;12(1-2):139-46 PMID: 17183221
  24. Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
    Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36 PMID: 7584402
  25. Predicting functionality of protein-DNA interactions by integrating diverse evidence.
    Bioinformatics. 2009 Jun 15;25(12):i137-44 PMID: 19477979
  26. The sigmaR regulon of Streptomyces coelicolor A32 reveals a key role in protein quality control during disulphide stress.
    Microbiology (Reading). 2010 Jun;156(Pt 6):1661-1672 PMID: 20185507
  27. Identification of the binding sites of regulatory proteins in bacterial genomes.
    Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11772-7 PMID: 12181488
  28. Pleiotropic functions of a Streptomyces pristinaespiralis autoregulator receptor in development, antibiotic biosynthesis, and expression of a superoxide dismutase.
    J Biol Chem. 2001 Nov 23;276(47):44297-306 PMID: 11557748
  29. Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference.
    Bioinformatics. 2004 Feb 12;20(3):407-15 PMID: 14960467
  30. Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces.
    Curr Opin Microbiol. 2010 Jun;13(3):263-73 PMID: 20303823
  31. Probabilistic inference of transcription factor concentrations and gene-specific regulatory activities.
    Bioinformatics. 2006 Nov 15;22(22):2775-81 PMID: 16966362
  32. WebLogo: a sequence logo generator.
    Genome Res. 2004 Jun;14(6):1188-90 PMID: 15173120
  33. The GOA database in 2009--an integrated Gene Ontology Annotation resource.
    Nucleic Acids Res. 2009 Jan;37(Database issue):D396-403 PMID: 18957448
  34. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents.
    Mol Cell Proteomics. 2004 Dec;3(12):1154-69 PMID: 15385600
  35. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2).
    Nature. 2002 May 9;417(6885):141-7 PMID: 12000953
  36. SIGffRid: a tool to search for sigma factor binding sites in bacterial genomes using comparative approach and biologically driven statistics.
    BMC Bioinformatics. 2008 Jan 31;9:73 PMID: 18237374
  37. Damped oscillations in the adaptive response of the iron homeostasis network of E. coli.
    Mol Microbiol. 2010 Apr;76(2):428-36 PMID: 20345668
  38. Statistical reconstruction of transcription factor activity using Michaelis-Menten kinetics.
    Biometrics. 2007 Sep;63(3):816-23 PMID: 17825013
  39. Mapping the DNA-binding domain and target sequences of the Streptomyces peucetius daunorubicin biosynthesis regulatory protein, DnrI.
    Mol Microbiol. 2002 Apr;44(2):449-60 PMID: 11972782
  40. Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes.
    Mol Microbiol. 2003 Jun;48(5):1289-303 PMID: 12787356
  41. The PII protein GlnK is a pleiotropic regulator for morphological differentiation and secondary metabolism in Streptomyces coelicolor.
    Appl Microbiol Biotechnol. 2011 Dec;92(6):1219-36 PMID: 22033567
  42. Target genes and structure of the direct repeats in the DNA-binding sequences of the response regulator PhoP in Streptomyces coelicolor.
    Nucleic Acids Res. 2008 Mar;36(4):1358-68 PMID: 18187507
  43. Network component analysis: reconstruction of regulatory signals in biological systems.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15522-7 PMID: 14673099
  44. Systems biology of antibiotic production by microorganisms.
    Nat Prod Rep. 2007 Dec;24(6):1262-87 PMID: 18033579
  45. Transcriptome dynamics-based operon prediction and verification in Streptomyces coelicolor.
    Nucleic Acids Res. 2007;35(21):7222-36 PMID: 17959654
  46. STAMP: a web tool for exploring DNA-binding motif similarities.
    Nucleic Acids Res. 2007 Jul;35(Web Server issue):W253-8 PMID: 17478497
  47. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  48. Analysis of differentially-regulated genes within a regulatory network by GPS genome navigation.
    Bioinformatics. 2005 Nov 15;21(22):4073-83 PMID: 16159917
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2012-07-00
Epub
2012-00-09
Pages
5227-39
Language
English
Region
England
NLM ID
0411011
PMCID
PMC3384326
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/F003498/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/FF003498/1 · United Kingdom
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