Regulatory networks allow organisms to match adaptive behavior to the complex and dynamic contingencies of their native habitats. Upon a sudden transition to a novel environment, the mismatch between the native behavior and the new niche provides selective pressure for adaptive evolution through mutations in elements that control gene expression. In the case of core components of cellular regulation and metabolism, with broad control over diverse biological processes, such mutations may have substantial pleiotropic consequences. Through extensive phenotypic analyses, we have characterized the systems-level consequences of one such mutation (rho*) in the global transcriptional terminator Rho of Escherichia coli. We find that a single amino acid change in Rho results in a massive change in the fitness landscape of the cell, with widely discrepant fitness consequences of identical single locus perturbations in rho* versus rhoWT backgrounds. Our observations reveal the extent to which a single regulatory mutation can transform the entire fitness landscape of the cell, causing a massive change in the interpretation of individual mutations and altering the evolutionary trajectories which may be accessible to a bacterial population.
Vyšlo v časopise: Fitness Landscape Transformation through a Single Amino Acid Change in the Rho Terminator. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002744 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002744
1. BurmannBMSchweimerKLuoXWahlMCStittBL 2010 A NusE∶NusG complex links transcription and translation. Science 328 501 504
2. EpshteinVDuttaDWadeJNudlerE 2010 An allosteric mechanism of Rho-dependent transcription termination. Nature 463 245 249
3. CardinaleCJWashburnRSTadigotlaVRBrownLMGottesmanME 2008 Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 320 935 938
4. PetersJMMooneyRAKuanPFRowlandJLKelesS 2009 Rho directs widespread termination of intragenic and stable RNA transcription. Proc Natl Acad Sci USA
5. WashburnRSGottesmanME 2010 Transcription termination maintains chromosome integrity. Proc Natl Acad Sci USA
6. DuttaDShatalinKEpshteinVGottesmanMENudlerE 2011 Linking rna polymerase backtracking to genome instability in E. coli. Cell 146 533 543
7. GoodarziHHottesAKTavazoieS 2009 Global discovery of adaptive mutations. Nat Methods 6 581 583
8. MartinezAOppermanTRichardsonJP 1996 Mutational analysis and secondary structure model of the RNP1-like sequence motif of transcription termination factor Rho. J Mol Biol 257 895 908
9. GoodarziHBennettBDAminiSReavesMLHottesAK 2010 Regulatory and metabolic rewiring during laboratory evolution of ethanol tolerance in E. coli. Mol Syst Biol 6 378
10. ConradTMLewisNEPalssonBO 2011 Microbial laboratory evolution in the era of genome-scale science. Mol Syst Biol 7 509
11. ConradTMJoyceARApplebeeMKBarrettCLXieB 2009 Whole-genome resequencing of Escherichia coli K-12 MG1655 undergoing short-term laboratory evolution in lactate minimal media reveals flexible selection of adaptive mutations. Genome Biol 10 R118
12. KishimotoTIijimaLTatsumiMOnoNOyakeA 2010 Transition from positive to neutral in mutation fixation along with continuing rising fitness in thermal adaptive evolution. PLoS Genet 6 e1001164 doi:10.1371/journal.pgen.1001164
13. TenaillonORodrguez-VerdugoAGautRLMcDonaldPBennettAF 2012 The molecular diversity of adaptive convergence. Science 335 457 461
14. PósfaiGPlunkettGFehérTFrischDKeilGM 2006 Emergent properties of reduced-genome Escherichia coli. Science 312 1044 1046
15. DornenburgJEDevitaAMPalumboMJWadeJT 2010 Widespread antisense transcription in escherichia coli. MBio 1
16. GoodarziHElementoOTavazoieS 2009 Revealing global regulatory perturbations across human cancers. Mol Cell 36 900 911
17. AshburnerMBallCABlakeJABotsteinDButlerH 2000 Gene ontology: tool for the unification of biology. the Gene Ontology Consortium. Nat Genet 25 25 29
18. GirgisHSHottesAKTavazoieS 2009 Genetic architecture of intrinsic antibiotic susceptibility. PLoS ONE 4 e5629 doi:10.1371/journal.pone.0005629
19. GirgisHSLiuYRyuWSTavazoieS 2007 A comprehensive genetic characterization of bacterial motility. PLoS Genet 3 e154 doi:10.1371/journal.pgen.0030154
20. HerringCDRaghunathanAHonischCPatelTApplebeeMK 2006 Comparative genome sequencing of escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet 38 1406 1412
21. ConradTMFrazierMJoyceARChoBKKnightEM 2010 Rna polymerase mutants found through adaptive evolution reprogram escherichia coli for optimal growth in minimal media. Proc Natl Acad Sci U S A 107 20500 20505
22. MurphyHCashelM 2003 Isolation of rna polymerase suppressors of a (p)ppgpp deficiency. Methods Enzymol 371 596 601
23. ApplebeeMKHerrgardMJPalssonBO 2008 Impact of individual mutations on increased fitness in adaptively evolved strains of escherichia coli. J Bacteriol 190 5087 5094
24. PhilippeNCrozatELenskiRESchneiderD 2007 Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 29 846 860
25. CrozatEPhilippeNLenskiREGeiselmannJSchneiderD 2005 Long-term experimental evolution in escherichia coli. xii. dna topology as a key target of selection. Genetics 169 523 532
26. WoodsRJBarrickJECooperTFShresthaUKauthMR 2011 Second-order selection for evolvability in a large escherichia coli population. Science 331 1433 1436
27. WagnerA 2005 Robustness and Evolvability in Living Systems (Princeton Studies in Complexity) Princeton University Press
28. DraghiJAParsonsTLWagnerGPPlotkinJB 2010 Mutational robustness can facilitate adaptation. Nature 463 353 355
29. RajonEMaselJ 2011 Evolution of molecular error rates and the consequences for evolvability. Proc Natl Acad Sci U S A 108 1082 1087
30. JaroszDFTaipaleMLindquistS 2010 Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu Rev Genet 44 189 216
31. ShorterJLindquistS 2005 Prions as adaptive conduits of memory and inheritance. Nat Rev Genet 6 435 450
32. HalfmannRLindquistS 2010 Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits. Science 330 629 632
33. HalfmannRAlbertiSLindquistS 2010 Prions, protein homeostasis, and phenotypic diversity. Trends Cell Biol 20 125 133
34. TyedmersJMadariagaMLLindquistS 2008 Prion switching in response to environmental stress. PLoS Biol 6 e294 doi:10.1371/journal.pbio.0060294
35. TrueHLLindquistSL 2000 A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407 477 483
36. Gama-CastroSSalgadoHPeralta-GilMSantos-ZavaletaAMuniz-RascadoL 2011 RegulonDB version 7.0: transcriptional regulation of Escherichia coli K-12 integrated within genetic sensory response units (Gensor Units). Nucl Acids Res 39 D98 D105
37. BlattnerFRPlunkettGBlochCAPernaNTBurlandV 1997 The complete genome sequence of Escherichia coli K-12. Science 277 1453 1462
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