Ancestral Genes Can Control the Ability of Horizontally Acquired Loci to Confer New Traits

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Horizontally acquired genes typically function as autonomous units conferring new abilities when introduced into different species. However, we reasoned that proteins preexisting in an organism might constrain the functionality of a horizontally acquired gene product if it operates on an ancestral pathway. Here, we determine how the horizontally acquired pmrD gene product activates the ancestral PmrA/PmrB two-component system in Salmonella enterica but not in the closely related bacterium Escherichia coli. The Salmonella PmrD protein binds to the phosphorylated PmrA protein (PmrA-P), protecting it from dephosphorylation by the PmrB protein. This results in transcription of PmrA-dependent genes, including those conferring polymyxin B resistance. We now report that the E. coli PmrD protein can activate the PmrA/PmrB system in Salmonella even though it cannot do it in E. coli, suggesting that these two species differ in an additional component controlling PmrA-P levels. We establish that the E. coli PmrB displays higher phosphatase activity towards PmrA-P than the Salmonella PmrB, and we identified a PmrB subdomain responsible for this property. Replacement of the E. coli pmrB gene with the Salmonella homolog was sufficient to render E. coli resistant to polymyxin B under PmrD-inducing conditions. Our findings provide a singular example whereby quantitative differences in the biochemical activities of orthologous ancestral proteins dictate the ability of a horizontally acquired gene product to confer species-specific traits. And they suggest that horizontally acquired genes can potentiate selection at ancestral loci.

Vyšlo v časopise: Ancestral Genes Can Control the Ability of Horizontally Acquired Loci to Confer New Traits. PLoS Genet 7(7): e32767. doi:10.1371/journal.pgen.1002184
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002184

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Zdroje

1. OchmanHLawrenceJGGroismanEA 2000 Lateral gene transfer and the nature of bacterial innovation. Nature 405 299 304

2. KuninVOuzounisCA 2003 The balance of driving forces during genome evolution in prokaryotes. Genome Res 13 1589 1594

3. SnelBBorkPHuynenMA 2002 Genomes in flux: the evolution of archaeal and proteobacterial gene content. Genome Res 12 17 25

4. LeratEDaubinVOchmanHMoranNA 2005 Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3 e130 doi:10.1371/journal.pbio.0030130

5. GogartenJPDoolittleWFLawrenceJG 2002 Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19 2226 2238

6. GogartenJPTownsendJP 2005 Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3 679 687

7. JainRRiveraMCMooreJELakeJA 2002 Horizontal gene transfer in microbial genome evolution. Theor Popul Biol 61 489 495

8. DobrindtUHochhutBHentschelUHackerJ 2004 Genomic islands in pathogenic and environmental microorganisms. Nat Rev Micro 2 414 424

9. McDanielTKKaperJB 1997 A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol 23 399 407

10. LercherMJPalC 2008 Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Mol Biol Evol 25 559 567

11. PalCPappBLercherMJ 2005 Horizontal gene transfer depends on gene content of the host. Bioinformatics 21 Suppl 2 ii222 223

12. KoxLFWostenMMGroismanEA 2000 A small protein that mediates the activation of a two-component system by another two-component system. EMBO J 19 1861 1872

13. GunnJSLimKBKruegerJKimKGuoL 1998 PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27 1171 1182

14. TrentMSRibeiroAALinSCotterRJRaetzCR 2001 An inner membrane enzyme in Salmonella and Escherichia coli that transfers 4-amino-4-deoxy-L-arabinose to lipid A: induction on polymyxin-resistant mutants and role of a novel lipid-linked donor. J Biol Chem 276 43122 43131

15. RolandKLMartinLEEstherCRSpitznagelJK 1993 Spontaneous pmrA mutants of Salmonella typhimurium LT2 define a new two-component regulatory system with a possible role in virulence. J Bacteriol 175 4154 4164

16. BreazealeSDRibeiroAARaetzCR 2002 Oxidative decarboxylation of UDP-glucuronic acid in extracts of polymyxin-resistant Escherichia coli. Origin of lipid A species modified with 4-amino-4-deoxy-L-arabinose. J Biol Chem 277 2886 2896

17. GroismanEAKayserJSonciniFC 1997 Regulation of polymyxin resistance and adaptation to low-Mg2+ environments. J Bacteriol 179 7040 7045

18. HerreraCMHankinsJVTrentMS 2010 Activation of PmrA inhibits LpxT-dependent phosphorylation of lipid A promoting resistance to antimicrobial peptides. Mol Microbiol 76 1444 1460

19. LeeHHsuFFTurkJGroismanEA 2004 The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica. J Bacteriol 186 4124 4133

20. SonciniFCGarcia VescoviESolomonFGroismanEA 1996 Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 178 5092 5099

21. KatoAGroismanEA 2004 Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes Dev 18 2302 2313

22. WostenMMKoxLFChamnongpolSSonciniFCGroismanEA 2000 A signal transduction system that responds to extracellular iron. Cell 103 113 125

23. WinfieldMDGroismanEA 2004 Phenotypic differences between Salmonella and Escherichia coli resulting from the disparate regulation of homologous genes. Proc Natl Acad Sci U S A 101 17162 17167

24. HagiwaraDYamashinoTMizunoT 2004 A Genome-wide view of the Escherichia coli BasS-BasR two-component system implicated in iron-responses. Biosci Biotechnol Biochem 68 1758 1767

25. MitrophanovAYJewettMWHadleyTJGroismanEA 2008 Evolution and dynamics of regulatory architectures controlling polymyxin B resistance in enteric bacteria. PLoS Genet 4 e1000233 doi:10.1371/journal.pgen.1000233

26. FoutsDETylerHLDeBoyRTDaughertySRenQ 2008 Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genet 4 e1000141 doi:10.1371/journal.pgen.1000141

27. ShinDLeeEJHuangHGroismanEA 2006 A positive feedback loop promotes transcription surge that jump-starts Salmonella virulence circuit. Science 314 1607 1609

28. WostenMMGroismanEA 1999 Molecular characterization of the PmrA regulon. J Biol Chem 274 27185 27190

29. KatoALatifiTGroismanEA 2003 Closing the loop: the PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD. Proc Natl Acad Sci U S A 100 4706 4711

30. NeuhardJNygaardP 1987 Purines and pyrimidines. NeidhardtFC Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology Washington, D.C. ASM Press 445 473

31. ShinDGroismanEA 2005 Signal-dependent binding of the response regulators PhoP and PmrA to their target promoters in vivo. J Biol Chem 280 4089 4094

32. MarinaAWaldburgerCDHendricksonWA 2005 Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24 4247 4259

33. ChampionKHigginsNP 2007 Growth rate toxicity phenotypes and homeostatic supercoil control differentiate Escherichia coli from Salmonella enterica serovar Typhimurium. J Bacteriol 189 5839 5849

34. MarchettiMCapelaDGlewMCruveillerSChane-Woon-MingB 2010 Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol 8 e1000280 doi:10.1371/journal.pbio.1000280

35. NakataNTobeTFukudaISuzukiTKomatsuK 1993 The absence of a surface protease, OmpT, determines the intercellular spreading ability of Shigella: the relationship between the ompT and kcpA loci. Mol Microbiol 9 459 468

36. DowellRDRyanOJansenACheungDAgarwalaS 2010 Genotype to phenotype: a complex problem. Science 328 469

37. HartmanJLtGarvikBHartwellL 2001 Principles for the buffering of genetic variation. Science 291 1001 1004

38. HoekstraHEHirschmannRJBundeyRAInselPACrosslandJP 2006 A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313 101 104

39. ShihVFKearnsJDBasakSSavinovaOVGhoshG 2009 Kinetic control of negative feedback regulators of NF-κB/RelA determines their pathogen- and cytokine-receptor signaling specificity. Proc Natl Acad Sci U S A 106 9619 9624

40. KholodenkoBN 2006 Cell-signalling dynamics in time and space. Nat Rev Mol Cell Biol 7 165 176

41. AlonU 2007 Network motifs: theory and experimental approaches. Nat Rev Genet 8 450 461

42. KatoAMitrophanovAYGroismanEA 2007 A connector of two-component regulatory systems promotes signal amplification and persistence of expression. Proc Natl Acad Sci U S A 104 12063 12068

43. WinfieldMDLatifiTGroismanEA 2005 Transcriptional regulation of the 4-amino-4-deoxy-L-arabinose biosynthetic genes in Yersinia pestis. J Biol Chem 280 14765 14772

44. ChamnongpolSDodsonWCromieMJHarrisZLGroismanEA 2002 Fe(III)-mediated cellular toxicity. Mol Microbiol 45 711 719

45. WinfieldMDGroismanEA 2003 Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol 69 3687 3694

46. StockAMRobinsonVLGoudreauPN 2000 Two-component signal transduction. Annu Rev Biochem 69 183 215

47. CasinoPRubioVMarinaA 2009 Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction. Cell 139 325 336

48. DuttaRYoshidaTInouyeM 2000 The critical role of the conserved Thr247 residue in the functioning of the osmosensor EnvZ, a histidine Kinase/Phosphatase, in Escherichia coli. J Biol Chem 275 38645 38653

49. HsingWRussoFDBerndKKSilhavyTJ 1998 Mutations that alter the kinase and phosphatase activities of the two-component sensor EnvZ. J Bacteriol 180 4538 4546

50. HsingWSilhavyTJ 1997 Function of conserved histidine-243 in phosphatase activity of EnvZ, the sensor for porin osmoregulation in Escherichia coli. J Bacteriol 179 3729 3735

51. ZhuYQinLYoshidaTInouyeM 2000 Phosphatase activity of histidine kinase EnvZ without kinase catalytic domain. Proc Natl Acad Sci U S A 97 7808 7813

52. ZhuYInouyeM 2002 The role of the G2 box, a conserved motif in the histidine kinase superfamily, in modulating the function of EnvZ. Mol Microbiol 45 653 663

53. FroelichJMTranKWallD 2006 A pmrA constitutive mutant sensitizes Escherichia coli to deoxycholic acid. J Bacteriol 188 1180 1183

54. GunnJS 2000 Mechanisms of bacterial resistance and response to bile. Microbes Infect 2 907 913

55. BoydEFWangFSWhittamTSSelanderRK 1996 Molecular genetic relationships of the salmonellae. Appl Environ Microbiol 62 804 808

56. OchmanHSelanderRK 1984 Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157 690 693

57. PalCPappBLercherMJ 2005 Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37 1372 1375

58. GouldSJ 1989 Wonderful Life. Norton, New York

59. BlountZDBorlandCZLenskiRE 2008 Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci U S A 105 7899 7906

60. SternDLOrgogozoV 2009 Is genetic evolution predictable? Science 323 746 751

61. StorzJFRunckAMSabatinoSJKellyJKFerrandN 2009 Evolutionary and functional insights into the mechanism underlying high-altitude adaptation of deer mouse hemoglobin. Proc Natl Acad Sci U S A 106 14450 14455

62. SnavelyMDMillerCGMaguireME 1991 The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem 266 815 823

63. MillerJH 1972 Experiments in molecular genetics: Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NY

64. DavisRWBolsteinDRothJR 1980 Advanced bacterial genetics: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

65. 2009 The Universal Protein Resource (UniProt) 2009. Nucleic Acids Res 37 D169 174

66. LarkinMABlackshieldsGBrownNPChennaRMcGettiganPA 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948

67. TamuraKDudleyJNeiMKumarS 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

68. WertzJEGoldstoneCGordonDMRileyMA 2003 A molecular phylogeny of enteric bacteria and implications for a bacterial species concept. J Evol Biol 16 1236 1248

69. KelleyLASternbergMJ 2009 Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4 363 371