Abstract
The structure and organization of 470 histidine biosynthetic genes from 47 different proteobacteria were combined with phylogenetic inference to investigate the mechanisms responsible for assembly of the his pathway and the origin of his operons. Data obtained in this work showed that a wide variety of different organization strategies of his gene arrays exist and that some his genes or entire his operons are likely to have been horizontally transferred between bacteria of the same or different proteobacterial branches. We propose a “piecewise” model for the origin and evolution of proteobacterial his operons, according to which the initially scattered his genes of the ancestor of proteobacteria coded for monofunctional enzymes (except possibly for hisD) and underwent a stepwise compacting process that reached its culmination in some γ-proteobacteria. The initial step of operon buildup was the formation of the his “core,” a cluster consisting of four genes (hisBHAF) whose products interconnect histidine biosynthesis to both de novo synthesis of purine metabolism and that occurred in the common ancestor of the α/β/γ branches, possibly after its separation from the ε one. The following step was the formation of three mini-operons (hisGDC, hisBHAF, hisIE) transcribed from independent promoters, that very likely occurred in the ancestor of the β/γ-branch, after its separation from the α one. Then the three mini-operons joined together to give a compact operon. In most γ-proteobacteria the two fusions involving the gene pairs hisN–B and hisI–E occurred. Finally the γ-proteobacterial his operon was horizontally transferred to other proteobacteria, such as Campylobacter jejuni. The biological significance of clustering of his genes is also discussed.
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P Alifano R Fani P Liò A Lazcano M Bazzicalupo MS Carlomagno CB Bruni (1996) ArticleTitleHistidine biosynthetic pathway and genes: structure, regulation and evolution Microbiol Rev 60 44–69 Occurrence Handle1:CAS:528:DyaK28XitVyrs7c%3D Occurrence Handle8852895
M Brill R Fani (2004a) ArticleTitleMolecular evolution of hisB genes J Mol Evol 58 225–237
M Brilli R Fani (2004b) ArticleTitleOrigin and evolution of eucaryal HIS7 genes: from metabolons to bifunctional proteins? Gene 339 149–160 Occurrence Handle1:CAS:528:DC%2BD2cXnsVKjurs%3D
S Dabizzi S Ammannato R Fani (2001) ArticleTitleExpression of horizontally transferred gene clusters: activation by promoter-generating mutations Res Microbiol 152 IssueID6 539–549 Occurrence Handle1:CAS:528:DC%2BD3MXms1Srs70%3D Occurrence Handle11501672
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
R Fani (2004) Gene duplication and gene loading RV Miller MJ Day (Eds) Microbial evolution: gene establishment, survival and exchange ASM Press Washington, DC 67–81
R Fani P Liò I Chiarelli M Bazzicalupo (1994) ArticleTitleThe evolution of the histidine biosynthetic genes in prokaryotes: a common ancestor for the hisA and hisF genes J Mol Evol 38 469–495
R Fani P Liò A Lazcano (1995) ArticleTitleMolecular evolution of the histidine biosynthetic pathway J Mol Evol 41 760–774 Occurrence Handle1:CAS:528:DyaK28XivFOjsQ%3D%3D Occurrence Handle8587121
R Fani E Tamburini E Mori A Lazcano P Liò C Barberio E Casalone D Cavalieri B Perito M Polsinelli (1997) ArticleTitleParalogous histidine biosynthetic genes: evolutionary analysis of the Saccharomyces cerevisiae HIS6 and HIS7 genes Gene 197 9– 17 Occurrence Handle1:CAS:528:DyaK2sXlsFGnu78%3D Occurrence Handle9332345
R Fani R Gallo S Fancelli E Mori E Tamburini A Lazcano (1998a) ArticleTitleHeterologous gene expression in an Escherichia coli population under starvation stress conditions J Mol Evol 47 363–368 Occurrence Handle1:CAS:528:DyaK1cXmt1amsrc%3D
R Fani E Mori E Tamburini A Lazcano (1998b) ArticleTitleEvolution of the structure and chromosomal distribution of histidine biosynthetic genes Orig Life Evol Biosph 28 IssueID4–6 555–570 Occurrence Handle1:CAS:528:DyaK1cXmtVWnsbs%3D
N Glansdorff (1999) ArticleTitleOn the origin of operons and their possible role in evolution toward thermophily J Mol Evol 49 432–438 Occurrence Handle1:CAS:528:DyaK1MXmslWhsLY%3D Occurrence Handle10486001
MA Huynen P Bork (1998) ArticleTitleMeasuring genome evolution Proc Natl Acad Sci USA 95 5849–5865 Occurrence Handle10.1073/pnas.95.11.5849 Occurrence Handle1:CAS:528:DyaK1cXjtlKhtbc%3D Occurrence Handle9600883
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 IssueID3 332–346 Occurrence Handle1:CAS:528:DyaK1MXhvVOqtL8%3D Occurrence Handle10331260
AB Kolsto (1997) ArticleTitleDynamic bacterial genome organization Mol Microbiol 24 IssueID2 241–248 Occurrence Handle1:STN:280:ByiA3czgvVQ%3D Occurrence Handle9159511
S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: molecular evolutionary genetics analysis software Bioinformatics 17 IssueID12 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241
F Jacob J Monod (1961) ArticleTitleGenetic regulatory mechanisms in the synthesis of proteins J Mol Biol 3 318–356 Occurrence Handle1:CAS:528:DyaF3MXhtFyrsLo%3D Occurrence Handle13718526
F Jacob D Perrin C Sanchez J Monod (1960) ArticleTitleL’opèron: groupe de gènes à expression cordonnée par un opératuer CR Acad Sci Paris 250 1727–1730 Occurrence Handle1:STN:280:CC%2BC2MfpsFM%3D
R Jensen (1996) Evolution of metabolic pathways in enteric bacteria FC Neidhart (Eds) Escherichia coli and Salmonella typhimurium ASM Press Washington, DC 2649–2662
A Lazcano GE Fox J Oro’ (1992) Life before DNA: the origin and evolution of early Archean cells RP Mortlock (Eds) The evolution of metabolic function CRC Press Boca Raton 237–339
JG Lawrence (1999) ArticleTitleGene transfer, speciation, and the evolution of bacterial genomes Curr Opin Microbiol 2 519–523 Occurrence Handle1:CAS:528:DyaK1MXntlCku70%3D Occurrence Handle10508729
JG Lawrence JR Roth (1996) ArticleTitleSelfish operons: horizontal transfer may drive the evolution of gene clusters Genetics 143 1843–1860 Occurrence Handle1:CAS:528:DyaK28XlvVSqt78%3D Occurrence Handle8844169
P Liò N Goldman J Thorne DT Jones (1998) ArticleTitleCombining protein secondary structure prediction and evolutionary inference Bioinformatics 14 726–733 Occurrence Handle9789098
WK Mass AJ Clark (1964) ArticleTitleStudies on the mechanism of repression of arginine biosynthesis in E.coli II. Dominance of repressibility in hybrids J Mol Biol 8 365–370
AR Mushegian EV Koonin (1996) ArticleTitleGene order is not conserved in bacterial evolution Trends Genet 12 289–290 Occurrence Handle1:CAS:528:DyaK28XkvV2rsr0%3D Occurrence Handle8783936
B Snel P Bork M Huynen (2000) ArticleTitleGenome evolution: Gene fusion versus gene fission Trends Genet 16 9–11 Occurrence Handle1:CAS:528:DC%2BD3cXlsFShsA%3D%3D Occurrence Handle10637623
Tamames J (2001) Evolution of gene order conservation in prokaryotes. Genome Biol 2(6) RESEARCH0020
JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res 22 IssueID22 4673–4680
Z Yang (1997) ArticleTitlePAML: a program package for phylogenetic analysis by maximum likelihood Comput Appl Biosci 13 IssueID5 555–556 Occurrence Handle1:CAS:528:DyaK2sXntlGnu7s%3D Occurrence Handle9367129
G Xie NO Keyhani CA Bonner RA Jensen (2003) ArticleTitleAncient origin of the tryptophan operon and the dynamics of evolutionary change Microbiol Mol Biol Rev 67 303–342 Occurrence Handle1:CAS:528:DC%2BD3sXnvF2nt7w%3D Occurrence Handle12966138
H Watanabe H Mori T Itoh T Gojobori (1997) ArticleTitleGenome plasticity as a paradigm for eubacteria evolution J Mol Evol 44 557–564
S Whelan N Goldman (2001) ArticleTitleA general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach Mol Biol Evol 18 691–699 Occurrence Handle1:CAS:528:DC%2BD3MXjtFyktr4%3D Occurrence Handle11319253
S Whelan P Liò N Goldman (2001) ArticleTitleMolecular phylogenetics: state-of-art methods for looking into the past Trends Genet 17 262–272 Occurrence Handle1:CAS:528:DC%2BD3MXjtFClu78%3D Occurrence Handle11335036
C Woese (1998) ArticleTitleThe universal ancestor Proc Natl Acad Sci USA 95 6854–6859 Occurrence Handle1:CAS:528:DyaK1cXjslynu7w%3D Occurrence Handle9618502
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Fani, R., Brilli, M. & Liò, P. The Origin and Evolution of Operons: The Piecewise Building of the Proteobacterial Histidine Operon. J Mol Evol 60, 378–390 (2005). https://doi.org/10.1007/s00239-004-0198-1
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DOI: https://doi.org/10.1007/s00239-004-0198-1