#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Adaptive Evolution of the Lactose Utilization Network in Experimentally Evolved Populations of


Adaptation to novel environments is often associated with changes in gene regulation. Nevertheless, few studies have been able both to identify the genetic basis of changes in regulation and to demonstrate why these changes are beneficial. To this end, we have focused on understanding both how and why the lactose utilization network has evolved in replicate populations of Escherichia coli. We found that lac operon regulation became strikingly variable, including changes in the mode of environmental response (bimodal, graded, and constitutive), sensitivity to inducer concentration, and maximum expression level. In addition, some classes of regulatory change were enriched in specific selective environments. Sequencing of evolved clones, combined with reconstruction of individual mutations in the ancestral background, identified mutations within the lac operon that recapitulate many of the evolved regulatory changes. These mutations conferred fitness benefits in environments containing lactose, indicating that the regulatory changes are adaptive. The same mutations conferred different fitness effects when present in an evolved clone, indicating that interactions between the lac operon and other evolved mutations also contribute to fitness. Similarly, changes in lac regulation not explained by lac operon mutations also point to important interactions with other evolved mutations. Together these results underline how dynamic regulatory interactions can be, in this case evolving through mutations both within and external to the canonical lactose utilization network.


Vyšlo v časopise: Adaptive Evolution of the Lactose Utilization Network in Experimentally Evolved Populations of. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002444
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002444

Souhrn

Adaptation to novel environments is often associated with changes in gene regulation. Nevertheless, few studies have been able both to identify the genetic basis of changes in regulation and to demonstrate why these changes are beneficial. To this end, we have focused on understanding both how and why the lactose utilization network has evolved in replicate populations of Escherichia coli. We found that lac operon regulation became strikingly variable, including changes in the mode of environmental response (bimodal, graded, and constitutive), sensitivity to inducer concentration, and maximum expression level. In addition, some classes of regulatory change were enriched in specific selective environments. Sequencing of evolved clones, combined with reconstruction of individual mutations in the ancestral background, identified mutations within the lac operon that recapitulate many of the evolved regulatory changes. These mutations conferred fitness benefits in environments containing lactose, indicating that the regulatory changes are adaptive. The same mutations conferred different fitness effects when present in an evolved clone, indicating that interactions between the lac operon and other evolved mutations also contribute to fitness. Similarly, changes in lac regulation not explained by lac operon mutations also point to important interactions with other evolved mutations. Together these results underline how dynamic regulatory interactions can be, in this case evolving through mutations both within and external to the canonical lactose utilization network.


Zdroje

1. CarrollSB 2005 Evolution at two levels: on genes and form. PLoS Biol 3 e245 doi:10.1371/journal.pbio.0030245

2. BornemanARGianoulisTAZhangZDYuHRozowskyJ 2007 Divergence of transcription factor binding sites across related yeast species. Science 317 815 819 doi:10.1126/science.1140748

3. WittkoppPJHaerumBKClarkAG 2008 Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet 40 346 350 doi:10.1038/ng.77

4. ZambranoMMSiegeleDAAlmirónMTormoAKolterR 1993 Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259 1757 1760

5. Notley-McRobbLFerenciT 1999 The generation of multiple co-existing mal-regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Environ Microbiol 1 45 52

6. CooperTFRozenDELenskiRE 2003 Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc Natl Acad Sci USA 100 1072 1077 doi:10.1073/pnas.0334340100

7. ChouH-HBerthetJMarxCJ 2009 Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. PLoS Genet 5 e1000652 doi:10.1371/journal.pgen.1000652

8. McDonaldMJGehrigSMMeintjesPLZhangX-XRaineyPB 2009 Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics 183 1041 1053 doi:10.1534/genetics.109.107110

9. WangLSpiraBZhouZFengLMaharjanRP 2010 Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol Evol 2 478 487 doi:10.1093/gbe/evq035

10. StoebelDMDormanCJ 2010 The effect of mobile element IS10 on experimental regulatory evolution in Escherichia coli. Mol Biol Evol 27 2105 2112 doi:10.1093/molbev/msq101

11. ZhongSKhodurskyADykhuizenDEDeanAM 2004 Evolutionary genomics of ecological specialization. Proc Natl Acad Sci USA 101 11719 11724 doi:10.1073/pnas.0404397101

12. SpencerCCBertrandMTravisanoMDoebeliM 2007 Adaptive diversification in genes that regulate resource use in Escherichia coli. PLoS Genet 3 e15 doi:10.1371/journal.pgen.0030015

13. CooperTFLenskiRE 2010 Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evol Biol 10 11 doi:10.1186/1471-2148-10-11

14. DekelEAlonU 2005 Optimality and evolutionary tuning of the expression level of a protein. Nature 436 588 592 doi:10.1038/nature03842

15. StoebelDMDeanAMDykhuizenDE 2008 The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178 1653 1660 doi:10.1534/genetics.107.085399

16. PerfeitoLGhozziSBergJSchnetzKLässigM 2011 Nonlinear fitness landscape of a molecular pathway. PLoS Genet 7 e1002160 doi:10.1371/journal.pgen.1002160

17. DykhuizenDEDeanAMHartlDL 1987 Metabolic flux and fitness. Genetics 115 25 31

18. SettyYmayoAESuretteMGAlonU 2003 Detailed map of a cis-regulatory input function. Proc Natl Acad Sci USA 100 7702 7707 doi:10.1073/pnas.1230759100

19. OzbudakEMThattaiMLimHNShraimanBIVan OudenaardenA 2004 Multistability in the lactose utilization network of Escherichia coli. Nature 427 737 740 doi:10.1038/nature02298

20. van HoekMHogewegP 2007 The effect of stochasticity on the lac operon: an evolutionary perspective. PLoS Comput Biol 3 e111 doi:10.1371/journal.pcbi.0030111

21. SantillánMMackeyMCZeronES 2007 Origin of bistability in the lac Operon. Biophys J 92 3830 3842 doi:10.1529/biophysj.106.101717

22. RobertLPaulGChenYTaddeiFBaiglD 2010 Pre-dispositions and epigenetic inheritance in the Escherichia coli lactose operon bistable switch. Mol Syst Biol 6 doi:10.1038/msb.2010.12

23. SavageauMA 1998 Demand theory of gene regulation. II. Quantitative application to the lactose and maltose operons of Escherichia coli. Genetics 149 1677 1691

24. GerlandUHwaT 2009 Evolutionary selection between alternative modes of gene regulation. Proc Natl Acad Sci USA 106 8841 8846 doi:10.1073/pnas.0808500106

25. SilverRSMatelesRI 1969 Control of mixed-substrate utilization in continuous cultures of Escherichia coli. J Bacteriol 97 535 543

26. DykhuizenDDaviesM 1980 An experimental model: bacterial specialists and generalists competing in chemostats. Ecology 61 1213 1227

27. NovickAWeinerM 1957 Enzyme Induction as an all-or-none phenomenon. Proc Natl Acad Sci USA 43 553 566

28. ChoiPJCaiLFriedaKXieXS 2008 A stochastic single-molecule event triggers phenotype switching of a bacterial cell. Science 322 442 446 doi:10.1126/science.1161427

29. KuhlmanTZhangZSaierMHHwaT 2007 Combinatorial transcriptional control of the lactose operon of Escherichia coli. Proc Natl Acad Sci USA 104 6043 6048 doi:10.1073/pnas.0606717104

30. CoulondreCMillerJHFarabaughPJGilbertW 1978 Molecular basis of base substitution hotspots in Escherichia coli. Nature 274 775 780

31. FarabaughPJSchmeissnerUHoferMMillerJH 1978 Genetic studies of the lac repressor. VII. On the molecular nature of spontaneous hotspots in the lacI gene of Escherichia coli. J Mol Biol 126 847 857

32. MarkiewiczPKleinaLGCruzCEhretSMillerJH 1994 Genetic studies of the lac repressor. XIV. Analysis of 4000 altered Escherichia coli lac repressors reveals essential and non-essential residues, as well as “spacers” which do not require a specific sequence. J Mol Biol 240 421 433 doi:10.1006/jmbi.1994.1458

33. BetzJLSasmorHMBuckFInsleyMYCaruthersMH 1986 Base substitution mutants of the lac operator: in vivo and in vitro affinities for lac repressor. Gene 50 123 132

34. MaquatLThorntonK 1980 lac promoter mutations located downstream from the transcription start site. J Mol Biol 139 537 549

35. MossingMCRecordMT 1985 Thermodynamic origins of specificity in the lac repressor-operator interaction. Adaptability in the recognition of mutant operator sites. J Mol Biol 186 295 305

36. FalconCMMatthewsKS 2000 Operator DNA sequence variation enhances high affinity binding by hinge helix mutants of lactose repressor protein. Biochemistry 39 11074 11083 doi:10.1021/bi000924z

37. KhanAIDinhDMSchneiderDLenskiRECooperTF 2011 Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332 1193 1196 doi:10.1126/science.1203801

38. BiggarSRCrabtreeGR 2001 Cell signaling can direct either binary or graded transcriptional responses. EMBO J 20 3167 3176 doi:10.1093/emboj/20.12.3167

39. InadaTKimataKAibaH 1996 Mechanism responsible for glucose-lactose diauxie in Escherichia coli: challenge to the cAMP model. Genes Cells 1 293 301

40. GörkeBStülkeJ 2008 Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Micro 6 613 624 doi:10.1038/nrmicro1932

41. MitchellARomanoGHGroismanBYonaADekelE 2009 Adaptive prediction of environmental changes by microorganisms. Nature 460 220 224 doi:10.1038/nature08112

42. LenskiRRoseMSimpsonS 1991 Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138 1315 1341

43. BertaniG 2004 Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J Bacteriol 186 595 600

44. ZaslaverABrenARonenMItzkovitzSKikoinI 2006 A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Meth 3 623 628 doi:10.1038/nmeth895

45. ChoiK-HGaynorJBWhiteKGLopezCBosioCM 2005 A Tn7-based broad-range bacterial cloning and expression system. Nat Meth 2 443 448 doi:10.1038/nmeth765

46. OehlerSEismannERKrämerHMüller-HillB 1990 The three operators of the lac operon cooperate in repression. EMBO J 9 973 979

47. StrackRLStronginDEBhattacharyyaDTaoWBermanA 2008 A noncytotoxic DsRed variant for whole-cell labeling. Nat Meth 5 955 957 doi:10.1038/nmeth.1264

48. FerrièresLHémeryGNhamTGuéroutA-MMazelD 2010 Silent mischief: bacteriophage Mu insertions contaminate products of Escherichia coli random mutagenesis performed using suicidal transposon delivery plasmids mobilized by broad-host-range RP4 conjugative machinery. J Bacteriol 192 6418 6427 doi:10.1128/JB.00621-10

49. MondsRDNewellPDGrossRHO'TooleGA 2007 Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol Microbiol 63 656 679 doi:10.1111/j.1365-2958.2006.05539.x

50. GentlemanRCCareyVJBatesDMBolstadBDettlingM 2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5 R80 doi:10.1186/gb-2004-5-10-r80

51. HahneFLeMeurNBrinkmanRREllisBHaalandP 2009 flowCore: a Bioconductor package for high throughput flow cytometry. BMC Bioinformatics 10 106 doi:10.1186/1471-2105-10-106

52. SarkarDLe MeurNGentlemanR 2008 Using flowViz to visualize flow cytometry data. Bioinformatics 24 878 879 doi:10.1093/bioinformatics/btn021

53. ZhangXBremerH 1995 Control of the Escherichia coli rrnB P1 promoter strength by ppGpp. J Biol Chem 270 11181 11189

54. FriesenMLSaxerGTravisanoMDoebeliM 2004 Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli. Evolution 58 245 260

55. PhilippeNAlcarazJ-PCoursangeEGeiselmannJSchneiderD 2004 Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 51 246 255 doi:10.1016/j.plasmid.2004.02.003

56. NghiemYCabreraMCupplesCGMillerJH 1988 The mutY gene: a mutator locus in Escherichia coli that generates GC to TA transversions. Proc Natl Acad Sci USA 85 2709 2713

57. SchaaperRMDanforthBNGlickmanBW 1986 Mechanisms of spontaneous mutagenesis: an analysis of the spectrum of spontaneous mutation in the Escherichia coli lacI gene. J Mol Biol 189 273 284

58. DrakeJW 1991 A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci USA 88 7160 7164

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#