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Evolutionary conservation of bacterial operons: does transcriptional connectivity matter?

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Abstract

In the literature, it has been frequently suggested that the connectivity of a protein, i.e., the number of proteins with which it interacts, is inversely correlated with the rate of evolution. We attempted to extrapolate from proteins to operons by testing the hypothesis that operons with high transcriptional connectivity, i.e., operons that are controlled through interactions with many transcription factors, are evolutionarily more conserved at the structure and sequence levels than low-connectivity operons. With Escherichia coli used as reference, two structural- and two sequence-conservation measures were determined for 82 groups of homologous operons from 30 completely-sequenced bacterial genomes. In E. coli, large operons tend to be regulated by more transcription factors than either smaller operons or single genes. Large E. coli operons that are regulated by single transcription factors were found to be regulated by activators more frequently than by repressors. Levels of sequence conservation and structural conservation of operons were found to be independent of each other, i.e., structurally conserved operons may be divergent in sequence, and vice versa. Transcriptional connectivity was found to influence neither sequence nor structural conservation of operons. Although this finding seems to contradict the situation in genes, a critical review of the literature indicates that although gene connectivity is frequently touted as a factor in determining rates of evolution, only a very small fraction of the variability in degrees of evolutionary conservation is explainable by this factor.

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References

  • J. Anba M. Bidaud M.L. Vasil A. Lazdunski (1990) ArticleTitleNucleotide sequence of the Pseudomonas aeruginosa phoB gene, the regulatory gene for the phosphate regulon J. Bacteriol. 172 4685–4689 Occurrence Handle1:CAS:528:DyaK3cXmt1Ghtbs%3D Occurrence Handle2115874

    CAS  PubMed  Google Scholar 

  • M.M Babu S.A Teichmann (2003) ArticleTitleFunctional determinants of transcription factors in Escherichia coli: protein families and binding sites Trends Genet. 19 75–79

    Google Scholar 

  • U. Bastolla M. Porto M.H. Eduardo Roman M.H. Vendruscolo (2003) ArticleTitleConnectivity of neutral networks, overdispersion & structural conservation in protein evolution J. Mol. Evol. 56 243–254 Occurrence Handle1:CAS:528:DC%2BD3sXhslWiu7g%3D Occurrence Handle12612828

    CAS  PubMed  Google Scholar 

  • H. Choy S. Adhya (1996) Negative Control in Escherichia coli and Salmonella, Cellular and Molecular Biology F.C. Neidhardt R. Curtiss J.L. Ingraham E.C.C. Lin K.B. Low (Eds) American Society for Microbiology Washington DC 1287–1299

    Google Scholar 

  • B. Clarke J.E. Mittenthal M. Senn (1993) ArticleTitleA model for the evolution of networks of genes J Theor. Biol. 165 269–289 Occurrence Handle1:CAS:528:DyaK2cXis1ejsrs%3D Occurrence Handle8114498

    CAS  PubMed  Google Scholar 

  • T. Dandekar B. Snel M. Huynen P. Bork (1998) ArticleTitleConservation of gene order: a fingerprint of proteins that physically interact Trends Biochem. Sci. 23 324–328 Occurrence Handle1:CAS:528:DyaK1cXmsVWmtrw%3D Occurrence Handle9787636

    CAS  PubMed  Google Scholar 

  • J. Felsenstein (1993) PHYLIP (Phylogeny Inference Package) version 3.5c. Department of Genetics University of Washington Seattle

    Google Scholar 

  • H.B. Fraser A.E. Hirsh L.M. Steinmetz C. Scharfe M.W. Feldman (2002) ArticleTitleEvolutionary rate in the protein interaction network Science 296 750–752 Occurrence Handle1:CAS:528:DC%2BD38XjtlOntrc%3D Occurrence Handle11976460

    CAS  PubMed  Google Scholar 

  • H.B. Fraser D.P. Wall A.E. Hirsh (2003) ArticleTitleA simple dependence between protein evolution rate and the number of protein-protein interactions BMC Evol. Biol. 3 11 Occurrence Handle12769820

    PubMed  Google Scholar 

  • D Graur WH Li (2000) Fundamentals of Molecular Evolution EditionNumber2 Sinauer Associates Sunderland, MA 481

    Google Scholar 

  • M.W. Hahn G.C. Conant A. Wagner (2004) ArticleTitleMolecular evolution in large genetic networks: does connectivity equal constraint? J. Mol. Evol. 58 203–211 Occurrence Handle1:CAS:528:DC%2BD2cXhvFOlsLw%3D Occurrence Handle15042341

    CAS  PubMed  Google Scholar 

  • D.G. Higgins J.D. Thompson T.J. Gibson (1996) ArticleTitleUsing CLUSTAL for multiple sequence alignments Meth. Enzymol. 266 383–402 Occurrence Handle1:CAS:528:DyaK28Xltl2nt7w%3D Occurrence Handle8743695

    CAS  PubMed  Google Scholar 

  • A.E. Hirsh H.B. Fraser (2001) ArticleTitleProtein dispensability and rate of evolution Nature 411 1046–1049 Occurrence Handle1:CAS:528:DC%2BD3MXltVCrsrs%3D Occurrence Handle11429604

    CAS  PubMed  Google Scholar 

  • M.A. Huynen P. Bork (1998) ArticleTitleMeasuring genome evolution Proc. Natl. Acad. Sci. USA 95 5849–5856 Occurrence Handle1:CAS:528:DyaK1cXjtlKhtbc%3D Occurrence Handle9600883

    CAS  PubMed  Google Scholar 

  • T. Itoh K. Takemoto H. Mori T. Gojobori (1999) ArticleTitleEvolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes Mol. Biol. Evol. 16 332–346 Occurrence Handle1:CAS:528:DyaK1MXhvVOqtL8%3D Occurrence Handle10331260

    CAS  PubMed  Google Scholar 

  • I.K. Jordan Y.I. Wolf E.V. Koonin (2003a) ArticleTitleCorrection No simple dependence between protein evolution rate and the number of protein-protein interactions: only the most prolific interactors tend to evolve slowly. BMC Evol. Biol. 3 5

    Google Scholar 

  • I.K. Jordan Y.I. Wolf E.V. Koonin (2003b) ArticleTitleNo simple dependence between protein evolution rate and the number of protein-protein interactions: only the most prolific interactors tend to evolve slowly BMC Evol. Biol. 3 1

    Google Scholar 

  • P.D. Karp M. Riley M. Saier I.T. Paulsen J. Collado-Vides (2002) ArticleTitleThe EcoCyc Database Nucleic Acids Res. 30 56–58 Occurrence Handle1:CAS:528:DC%2BD38Xht12ktr0%3D Occurrence Handle11752253

    CAS  PubMed  Google Scholar 

  • D.M. Krylov Y.I. Wolf I.B. Rogozin E.V. Koonin (2003) ArticleTitleGene loss, protein sequence divergence, gene dispensability, expression level & interactivity are correlated in eukaryotic evolution Genome Res. 13 2229–2235 Occurrence Handle1:CAS:528:DC%2BD3sXotF2hsL0%3D Occurrence Handle14525925

    CAS  PubMed  Google Scholar 

  • W.C. LatheIII B. Snel P. Bork (2000) ArticleTitleGene context conservation of a higher order than operons Trends Biochem. Sci. 25 474–479

    Google Scholar 

  • W.K. Maas A.J. Clark (1964) ArticleTitleStudies on the mechanism of repression of arginine biosynthesis in E. coli. II. Dominance of repressibility in diploids J. Mol. Biol. 8 365–370 Occurrence Handle1:CAS:528:DyaF2cXnslagsA%3D%3D

    CAS  Google Scholar 

  • K. Makino H. Shinagawa M. Amemura A. Nakata (1986) ArticleTitleNucleotide sequence of the pho B gene, the positive regulatory gene for the phosphate regulon of Escherichia coli K-12 J. Mol. Biol. 190 37–44 Occurrence Handle1:CAS:528:DyaL28Xlt1yntLo%3D Occurrence Handle3537313

    CAS  PubMed  Google Scholar 

  • A. Martinez-Antonio J. Collado-Vides (2003) ArticleTitleIdentifying global regulators in transcriptional regulatory networks in bacteria Curr. Opin. Microbiol. 6 482–489 Occurrence Handle1:CAS:528:DC%2BD3sXot12hsbo%3D Occurrence Handle14572541

    CAS  PubMed  Google Scholar 

  • A.R. Mushegian E.V. Koonin (1996) ArticleTitleGene order is not conserved in bacterial evolution Trends Genet. 12 289–290 Occurrence Handle1:CAS:528:DyaK28XkvV2rsr0%3D Occurrence Handle8783936

    CAS  PubMed  Google Scholar 

  • C. Pal B. Papp L.D. Hurst (2001) ArticleTitleHighly expressed genes in yeast evolve slowly Genetics 158 927–931 Occurrence Handle1:CAS:528:DC%2BD3MXltFSitr4%3D Occurrence Handle11430355

    CAS  PubMed  Google Scholar 

  • Z. Pragai N.E. Allenby N. O‘Connor S. Dubrac G. Rapoport (2004) ArticleTitleTranscriptional regulation of the phoPR operon in Bacillus subtilis J. Bacteriol. 186 1182–1190 Occurrence Handle1:CAS:528:DC%2BD2cXhsVWjtLc%3D Occurrence Handle14762014

    CAS  PubMed  Google Scholar 

  • H. Salgado A. Santos-Zavaleta S. Gama-Castro D. Millan-Zarate F.R. Blattner (2000) ArticleTitleRegulonDB (version 3.0): Transcriptional regulation and operon organization in Escherichia coli K-12 Nucleic Acids Res. 28 65–67 Occurrence Handle1:CAS:528:DC%2BD3cXhvVGqu7c%3D Occurrence Handle10592182

    CAS  PubMed  Google Scholar 

  • H. Salgado S. Gama-Castro A. Martinez-Antonio E. Diaz-Peredo F. Sanchez-Solano (2004) ArticleTitleRegulonDB (version 4.0): transcriptional regulation, operon organization and growth conditions in Escherichia coli K-12 Nucleic Acids Res. 32 D303–D306 Occurrence Handle1:CAS:528:DC%2BD3sXhtVSru7nJ Occurrence Handle14681419

    CAS  PubMed  Google Scholar 

  • S.S. Shen-Orr R. Milo S. Mangan U. Alon (2002) ArticleTitleNetwork motifs in the transcriptional regulation network of Escherichia coli Nat. Genet. 31 64–68 Occurrence Handle1:CAS:528:DC%2BD38Xjt1Kns70%3D Occurrence Handle11967538

    CAS  PubMed  Google Scholar 

  • J.L. Siefert K.A. Martin F. Abdi W.R. Widger G.E. Fox (1997) ArticleTitleConserved gene clusters in bacterial genomes provide further support for the primacy of RNA J Mol. Evol. 45 467–472 Occurrence Handle1:CAS:528:DyaK2sXmvFSkt7k%3D Occurrence Handle9342394

    CAS  PubMed  Google Scholar 

  • R.L. Tatusov E.V. Koonin D.J. Lipman (1997) ArticleTitleA genomic perspective on protein families Science 278 631–637 Occurrence Handle1:CAS:528:DyaK2sXmvVOrsL0%3D Occurrence Handle9381173

    CAS  PubMed  Google Scholar 

  • R.L. Tatusov D.A. Natale I.V. Garkavtsev T.A. Tatusova U.T. Shankavaram (2001) ArticleTitleThe COG database: new developments in phylogenetic classification of proteins from complete genomes Nucleic Acids Res. 29 22–28 Occurrence Handle1:CAS:528:DC%2BD3MXjtlWnsLo%3D Occurrence Handle11125040

    CAS  PubMed  Google Scholar 

  • M. Thattai A. van Oudenaarden (2001) ArticleTitleIntrinsic noise in gene regulatory networks Proc. Natl. Acad. Sci. USA 98 8614–8619 Occurrence Handle1:CAS:528:DC%2BD3MXls1Witrk%3D Occurrence Handle11438714

    CAS  PubMed  Google Scholar 

  • D., A. Thieffry M. Huerta E. Perez-Rueda J. Collado-Vides (1998) ArticleTitleFrom specific gene regulation to genomic networks: a global analysis of transcriptional regulation in Escherichia coli Bioessays 20 433–440 Occurrence Handle1:STN:280:DyaK1czjsFCksA%3D%3D Occurrence Handle9670816

    CAS  PubMed  Google Scholar 

  • W.M.A. von Kruger S. Humphreys J.M. Ketley (1999) ArticleTitleA role for the PhoBR regulatory system homologue in the Vibrio cholerae phosphate-limitation response and intestinal colonization Microbiology 145 2463–2475 Occurrence Handle1:CAS:528:DyaK1MXmsVyhtLo%3D Occurrence Handle10517599

    CAS  PubMed  Google Scholar 

  • B.L. Wanner (1993) ArticleTitleGene regulation by phosphate in enteric bacteria J. Cell Biochem. 51 47–54 Occurrence Handle1:CAS:528:DyaK3sXht1SmsL4%3D Occurrence Handle8432742

    CAS  PubMed  Google Scholar 

  • B.L. Wanner B.D. Chang (1987) ArticleTitle The phoBR operon in Escherichia coli K-12 J. Bacteriol. 169 5569–5574 Occurrence Handle1:CAS:528:DyaL1cXhslSitQ%3D%3D Occurrence Handle2824439

    CAS  PubMed  Google Scholar 

  • H. Watanabe H. Mori T. Itoh T. Gojobori (1997) ArticleTitleGenome plasticity as a paradigm of eubacteria evolution J. Mol. Evol. 44 S57–64 Occurrence Handle1:CAS:528:DyaK2sXhsFGrtrs%3D Occurrence Handle9395406

    CAS  PubMed  Google Scholar 

  • E.J. Williams L.D. Hurst (2000) ArticleTitleThe proteins of linked genes evolve at similar rates Nature 407 900–903 Occurrence Handle1:CAS:528:DC%2BD3cXns1Omtbk%3D Occurrence Handle11057667

    CAS  PubMed  Google Scholar 

  • A.C. Wilson S.S. Carlson T.J. White (1977) ArticleTitleBiochemical evolution Annu. Rev. Biochem. 46 573–639 Occurrence Handle1:CAS:528:DyaE2sXltFehsrY%3D Occurrence Handle409339

    CAS  PubMed  Google Scholar 

  • Y.I. Wolf I.B. Rogozin A.S. Kondrashov E.V. Koonin (2001) ArticleTitleGenome alignment, evolution of prokaryotic genome organization & prediction of gene function using genomic context Genome Res. 11 356–372 Occurrence Handle1:CAS:528:DC%2BD3MXhvVOnsbg%3D Occurrence Handle11230160

    CAS  PubMed  Google Scholar 

  • Y.I. Wolf G. Karev E.V. Koonin (2002) ArticleTitleScale-free networks in biology: new insights into the fundamentals of evolution? Bioessays 24 105–109 Occurrence Handle11835273

    PubMed  Google Scholar 

  • I. Yanai J.C. Mellor C. DeLisi (2002) ArticleTitleIdentifying functional links between genes using conserved chromosomal proximity Trends Genet. 18 176–179 Occurrence Handle1:CAS:528:DC%2BD38XisV2htLs%3D Occurrence Handle11932011

    CAS  PubMed  Google Scholar 

  • J. Yang Z. Gu W.H. Li (2003) ArticleTitleRate of protein evolution versus fitness effect of gene deletion Mol. Biol. Evol. 20 772–774 Occurrence Handle12679525

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, 69978, Israel

    Einat Hazkani-Covo & Dan Graur

  2. Department of Biology and Biochemistry, University of Houston, Houston, 77204, TX, USA

    Dan Graur

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  1. Einat Hazkani-Covo
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  2. Dan Graur
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Correspondence to Dan Graur.

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Hazkani-Covo, E., Graur, D. Evolutionary conservation of bacterial operons: does transcriptional connectivity matter?. Genetica 124, 145–166 (2005). https://doi.org/10.1007/s10709-005-0950-5

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  • DOI: https://doi.org/10.1007/s10709-005-0950-5

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