Silencing by H-NS Potentiated the Evolution of
H-NS is an abundant DNA-binding protein found in enteric bacteria including the important pathogens Escherichia, Salmonella, Vibrio, and Yersinia, that plays a primary role in defending the bacterial genome by silencing AT-rich foreign genes. H-NS has been hypothesized to facilitate the evolution of bacterial species by acting as a buffer against the negative consequences that can occur when new genes are incorporated into pre-existing genetic landscapes. Here experimental evolution and whole-genome sequencing were employed to determine the factors underlying the severe growth defects displayed by Salmonella strains lacking H-NS. Through tracking the evolution of several independently derived mutant lineages, we find that compensatory mutations arise quickly and that they occur in loci related to virulence. A frequent outcome was loss of the Salmonella Pathogenicity Island-1, the defining genetic island of the genus Salmonella. Among other things these findings demonstrate that H-NS has enabled the birth of a new and important bacterial pathogen by buffering the fitness consequences caused by overexpression of SPI-1. These findings are likely generalizable to pathogens such as E. coli, Yersinia, Shigella, and Vibrio cholerae, all of which maintain a pool of “expensive” AT-rich virulence genes that are repressed by H-NS.
Vyšlo v časopise:
Silencing by H-NS Potentiated the Evolution of. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004500
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004500
Souhrn
H-NS is an abundant DNA-binding protein found in enteric bacteria including the important pathogens Escherichia, Salmonella, Vibrio, and Yersinia, that plays a primary role in defending the bacterial genome by silencing AT-rich foreign genes. H-NS has been hypothesized to facilitate the evolution of bacterial species by acting as a buffer against the negative consequences that can occur when new genes are incorporated into pre-existing genetic landscapes. Here experimental evolution and whole-genome sequencing were employed to determine the factors underlying the severe growth defects displayed by Salmonella strains lacking H-NS. Through tracking the evolution of several independently derived mutant lineages, we find that compensatory mutations arise quickly and that they occur in loci related to virulence. A frequent outcome was loss of the Salmonella Pathogenicity Island-1, the defining genetic island of the genus Salmonella. Among other things these findings demonstrate that H-NS has enabled the birth of a new and important bacterial pathogen by buffering the fitness consequences caused by overexpression of SPI-1. These findings are likely generalizable to pathogens such as E. coli, Yersinia, Shigella, and Vibrio cholerae, all of which maintain a pool of “expensive” AT-rich virulence genes that are repressed by H-NS.
Zdroje
1. OchmanH, LawrenceJG, GroismanEA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299–304.
2. WaldorMK, MekalanosJJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910–1914.
3. de la CruzF, DaviesJ (2000) Horizontal gene transfer and the origin of species: lessons from bacteria. Trends in microbiology 8: 128–133.
4. LesicB, CarnielE (2005) Horizontal transfer of the high-pathogenicity island of Yersinia pseudotuberculosis. Journal of bacteriology 187: 3352–3358.
5. BecqJ, GutierrezMC, Rosas-MagallanesV, RauzierJ, GicquelB, et al. (2007) Contribution of horizontally acquired genomic islands to the evolution of the tubercle bacilli. Molecular biology and evolution 24: 1861–1871.
6. PrerakDT, PorwollikS, LongF, ChengP, WollamA, et al. (2013) Evolutionary Genomics of Salmonella enterica Subspecies. mBio 4: e00198–00113.
7. WinterSE, ThiennimitrP, WinterMG, ButlerBP, HusebyDL, et al. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467: 426–429.
8. FookesM, SchroederGN, LangridgeGC, BlondelCJ, MamminaC, et al. (2011) Salmonella bongori provides insights into the evolution of the Salmonellae. PLoS pathogens 7: e1002191.
9. MillsDM, BajajV, LeeCA (1995) A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol 15: 749–759.
10. GroismanEA, OchmanH (1993) Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. Embo J 12: 3779–3787.
11. GalanJE, CurtissR3rd (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A 86: 6383–6387.
12. GalanJE, ZhouD (2000) Striking a balance: modulation of the actin cytoskeleton by Salmonella. Proc Natl Acad Sci U S A 97: 8754–8761.
13. BaltrusDA (2013) Exploring the costs of horizontal gene transfer. Trends in ecology & evolution 28: 489–95.
14. SorekR, ZhuY, CreeveyCJ, FrancinoMP, BorkP, et al. (2007) Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318: 1449–1452.
15. ParkC, ZhangJ (2012) High expression hampers horizontal gene transfer. Genome biology and evolution 4: 523–532.
16. ZhengH, LuL, WangB, PuS, ZhangX, et al. (2008) Genetic basis of virulence attenuation revealed by comparative genomic analysis of Mycobacterium tuberculosis strain H37Ra versus H37Rv. PloS one 3: e2375.
17. PasteurL (1881) Sur les virus-vaccins du cholera des poules et du charbon. CR Travaux Congr Int Dir Stn Agron Sess Versailles 151–162.
18. PlattTG, BeverJD, FuquaC (2012) A cooperative virulence plasmid imposes a high fitness cost under conditions that induce pathogenesis. Proceedings Biological sciences/The Royal Society 279: 1691–1699.
19. SchuchR, MaurelliAT (1997) Virulence plasmid instability in Shigella flexneri 2a is induced by virulence gene expression. Infection and immunity 65: 3686–3692.
20. SchuchR, MaurelliAT (1997) Virulence plasmid instability in Shigella flexneri 2a is induced by virulence gene expression. Infect Immun 65: 3686–3692.
21. LucchiniS, RowleyG, GoldbergMD, HurdD, HarrisonM, et al. (2006) H-NS Mediates the Silencing of Laterally Acquired Genes in Bacteria. PLoS Pathog 2: e81.
22. NavarreWW, PorwollikS, WangY, McClellandM, RosenH, et al. (2006) Selective Silencing of Foreign DNA with Low GC Content by the H-NS Protein in Salmonella. Science 313: 236–238.
23. OshimaT, IshikawaS, KurokawaK, AibaH, OgasawaraN (2006) Escherichia coli Histone-Like Protein H-NS Preferentially Binds to Horizontally Acquired DNA in Association with RNA Polymerase. DNA Res 13: 141–153.
24. GraingerDC, HurdD, GoldbergMD, BusbySJ (2006) Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34: 4642–4652.
25. BanosRC, ViveroA, AznarS, GarciaJ, PonsM, et al. (2009) Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS. PLoS Genet 5: e1000513.
26. SinghSS, SinghN, BonocoraRP, FitzgeraldDM, WadeJT, et al. (2014) Widespread suppression of intragenic transcription initiation by H-NS. Genes Dev 28: 214–219.
27. GordonBR, LiY, CoteA, WeirauchMT, DingP, et al. (2011) Structural basis for recognition of AT-rich DNA by unrelated xenogeneic silencing proteins. Proc Natl Acad Sci U S A 108: 10690–10695.
28. SetteM, SpurioR, TrottaE, BrandiziC, BrandiA, et al. (2009) Sequence-specific recognition of DNA by the C-terminal domain of nucleoid-associated protein H-NS. J Biol Chem 284: 30453–30462.
29. UeguchiC, SuzukiT, YoshidaT, TanakaK, MizunoT (1996) Systematic mutational analysis revealing the functional domain organization of Escherichia coli nucleoid protein H-NS. J Mol Biol 263: 149–162.
30. AroldST, LeonardPG, ParkinsonGN, LadburyJE (2010) H-NS forms a superhelical protein scaffold for DNA condensation. Proc Natl Acad Sci U S A 107: 15728–15732.
31. BadautC, WilliamsR, ArluisonV, BouffartiguesE, RobertB, et al. (2002) The degree of oligomerization of the H-NS nucleoid structuring protein is related to specific binding to DNA. J Biol Chem 277: 41657–41666.
32. BouffartiguesE, BuckleM, BadautC, TraversA, RimskyS (2007) H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing. Nat Struct Mol Biol 14: 441–448.
33. GroismanEA, OchmanH (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87: 791–794.
34. NavarreWW, McClellandM, LibbySJ, FangFC (2007) Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev 21: 1456–1471.
35. DaubinV, LeratE, PerriereG (2003) The source of laterally transferred genes in bacterial genomes. Genome Biol 4: R57.
36. Vallet-GelyI, DonovanKE, FangR, JoungJK, DoveSL (2005) Repression of phase-variable cup gene expression by H-NS-like proteins in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 102: 11082–11087.
37. GordonBR, ImperialR, WangL, NavarreWW, LiuJ (2008) Lsr2 of Mycobacterium represents a novel class of H-NS-like proteins. J Bacteriol 190: 7052–7059.
38. BanosRC, PonsJI, MadridC, JuarezA (2008) A global modulatory role for the Yersinia enterocolitica H-NS protein. Microbiology 154: 1281–1289.
39. CastangS, McManusHR, TurnerKH, DoveSL (2008) H-NS family members function coordinately in an opportunistic pathogen. Proc Natl Acad Sci U S A 105: 18947–18952.
40. GordonBR, LiY, WangL, SintsovaA, van BakelH, et al. (2010) Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 107: 5154–5159.
41. CastangS, DoveSL (2012) Basis for the essentiality of H-NS family members in Pseudomonas aeruginosa. J Bacteriol 194: 5101–5109.
42. HerovenAK, NagelG, TranHJ, ParrS, DerschP (2004) RovA is autoregulated and antagonizes H-NS-mediated silencing of invasin and rovA expression in Yersinia pseudotuberculosis. Mol Microbiol 53: 871–888.
43. EllisonDW, MillerVL (2006) H-NS Represses inv Transcription in Yersinia enterocolitica through Competition with RovA and Interaction with YmoA. J Bacteriol 188: 5101–5112.
44. DameRT, LuijsterburgMS, KrinE, BertinPN, WagnerR, et al. (2005) DNA bridging: a property shared among H-NS-like proteins. J Bacteriol 187: 1845–1848.
45. ZhangA, RimskyS, ReabanME, BucH, BelfortM (1996) Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. Embo J 15: 1340–1349.
46. SonnenfieldJM, BurnsCM, HigginsCF, HintonJC (2001) The nucleoid-associated protein StpA binds curved DNA, has a greater DNA-binding affinity than H-NS and is present in significant levels in hns mutants. Biochimie 83: 243–249.
47. UyarE, KurokawaK, YoshimuraM, IshikawaS, OgasawaraN, et al. (2009) Differential binding profiles of StpA in wild-type and h-ns mutant cells: a comparative analysis of cooperative partners by chromatin immunoprecipitation-microarray analysis. J Bacteriol 191: 2388–2391.
48. LucchiniS, McDermottP, ThompsonA, HintonJC (2009) The H-NS-like protein StpA represses the RpoS (sigma 38) regulon during exponential growth of Salmonella Typhimurium. Mol Microbiol 74: 1169–1186.
49. WilliamsRM, RimskyS, BucH (1996) Probing the structure, function, and interactions of the Escherichia coli H-NS and StpA proteins by using dominant negative derivatives. J Bacteriol 178: 4335–4343.
50. JohanssonJ, ErikssonS, SondenB, WaiSN, UhlinBE (2001) Heteromeric interactions among nucleoid-associated bacterial proteins: localization of StpA-stabilizing regions in H-NS of Escherichia coli. J Bacteriol 183: 2343–2347.
51. DeighanP, BeloinC, DormanCJ (2003) Three-way interactions among the Sfh, StpA and H-NS nucleoid-structuring proteins of Shigella flexneri 2a strain 2457T. Mol Microbiol 48: 1401–1416.
52. CusickME, BelfortM (1998) Domain structure and RNA annealing activity of the Escherichia coli regulatory protein StpA. Mol Microbiol 28: 847–857.
53. DeighanP, FreeA, DormanCJ (2000) A role for the Escherichia coli H-NS-like protein StpA in OmpF porin expression through modulation of micF RNA stability. Mol Microbiol 38: 126–139.
54. SondénB, UhlinBE (1996) Coordinated and differential expression of histone-like proteins in Escherichia coli: regulation and function of the H-NS analog StpA. Embo J 15: 4970–4980.
55. FreeA, DormanCJ (1997) The Escherichia coli stpA gene is transiently expressed during growth in rich medium and is induced in minimal medium and by stress conditions. J Bacteriol 179: 909–918.
56. JohanssonJ, UhlinBE (1999) Differential protease-mediated turnover of H-NS and StpA revealed by a mutation altering protein stability and stationary-phase survival of Escherichia coli. Proc Natl Acad Sci U S A 96: 10776–10781.
57. Ali AzamT, IwataA, NishimuraA, UedaS, IshihamaA (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181: 6361–6370.
58. BattestiA, TsegayeYM, PackerDG, MajdalaniN, GottesmanS (2012) H-NS regulation of IraD and IraM antiadaptors for control of RpoS degradation. Journal of bacteriology 194: 2470–2478.
59. GunnJS, Alpuche-ArandaCM, LoomisWP, BeldenWJ, MillerSI (1995) Characterization of the Salmonella typhimurium pagC/pagD chromosomal region. J Bacteriol 177: 5040–5047.
60. PerezJC, LatifiT, GroismanEA (2008) Overcoming H-NS-mediated transcriptional silencing of horizontally acquired genes by the PhoP and SlyA proteins in Salmonella enterica. J Biol Chem 283: 10773–10783.
61. van VelkinburghJC, GunnJS (1999) PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect Immun 67: 1614–1622.
62. SonciniFC, GroismanEA (1996) Two-component regulatory systems can interact to process multiple environmental signals. J Bacteriol 178: 6796–6801.
63. GunnJS, MillerSI (1996) PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J Bacteriol 178: 6857–6864.
64. GroismanEA, KayserJ, SonciniFC (1997) Regulation of polymyxin resistance and adaptation to low-Mg2+ environments. J Bacteriol 179: 7040–7045.
65. PangPP, LundbergAS, WalkerGC (1985) Identification and characterization of the mutL and mutS gene products of Salmonella typhimurium LT2. J Bacteriol 163: 1007–1015.
66. MarinusMG (2010) DNA methylation and mutator genes in Escherichia coli K-12. Mutat Res 705: 71–76.
67. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
68. ZerbinoDR, BirneyE (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.
69. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.
70. GolubevaYA, SadikAY, EllermeierJR, SlauchJM (2012) Integrating global regulatory input into the Salmonella pathogenicity island 1 type III secretion system. Genetics 190: 79–90.
71. BertinP, TeraoE, LeeEH, LejeuneP, ColsonC, et al. (1994) The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J Bacteriol 176: 5537–5540.
72. SoutourinaO, KolbA, KrinE, Laurent-WinterC, RimskyS, et al. (1999) Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol 181: 7500–7508.
73. KoM, ParkC (2000) Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J Mol Biol 303: 371–382.
74. PaulK, CarlquistWC, BlairDF (2011) Adjusting the spokes of the flagellar motor with the DNA-binding protein H-NS. J Bacteriol 193: 5914–5922.
75. BertinP, HommaisF, KrinE, SoutourinaO, TendengC, et al. (2001) H-NS and H-NS-like proteins in Gram-negative bacteria and their multiple role in the regulation of bacterial metabolism. Biochimie 83: 235–241.
76. SturmA, HeinemannM, ArnoldiniM, BeneckeA, AckermannM, et al. (2011) The cost of virulence: retarded growth of Salmonella Typhimurium cells expressing type III secretion system 1. PLoS Pathog 7: e1002143.
77. BlockerA, KomoriyaK, AizawaS (2003) Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc Natl Acad Sci U S A 100: 3027–3030.
78. GinocchioCC, RahnK, ClarkeRC, GalanJE (1997) Naturally occurring deletions in the centisome 63 pathogenicity island of environmental isolates of Salmonella spp. Infect Immun 65: 1267–1272.
79. DiardM, GarciaV, MaierL, Remus-EmsermannMN, RegoesRR, et al. (2013) Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature 494: 353–356.
80. MurakamiKS (2013) X-ray crystal structure of Escherichia coli RNA polymerase sigma70 holoenzyme. J Biol Chem 288: 9126–9134.
81. ZhangY, FengY, ChatterjeeS, TuskeS, HoMX, et al. (2012) Structural basis of transcription initiation. Science 338: 1076–1080.
82. AznarS, PaytubiS, JuarezA (2013) The Hha protein facilitates incorporation of horizontally acquired DNA in enteric bacteria. Microbiology 159: 545–554.
83. De BiaseD, TramontiA, BossaF, ViscaP (1999) The response to stationary-phase stress conditions in Escherichia coli: role and regulation of the glutamic acid decarboxylase system. Mol Microbiol 32: 1198–1211.
84. RajkumariK, GowrishankarJ (2001) In vivo expression from the RpoS-dependent P1 promoter of the osmotically regulated proU operon in Escherichia coli and Salmonella enterica serovar Typhimurium: activation by rho and hns mutations and by cold stress. J Bacteriol 183: 6543–6550.
85. ShinM, SongM, RheeJH, HongY, KimYJ, et al. (2005) DNA looping-mediated repression by histone-like protein H-NS: specific requirement of Esigma70 as a cofactor for looping. Genes Dev 19: 2388–2398.
86. GraingerDC, GoldbergMD, LeeDJ, BusbySJ (2008) Selective repression by Fis and H-NS at the Escherichia coli dps promoter. Mol Microbiol 68: 1366–1377.
87. YamashinoT, UeguchiC, MizunoT (1995) Quantitative control of the stationary phase-specific sigma factor, sigma S, in Escherichia coli: involvement of the nucleoid protein H-NS. Embo J 14: 594–602.
88. ZhouY, GottesmanS (2006) Modes of regulation of RpoS by H-NS. J Bacteriol 188: 7022–7025.
89. MelliesJL, LarabeeFJ, ZarrMA, HorbackKL, LorenzenE, et al. (2008) Ler interdomain linker is essential for anti-silencing activity in enteropathogenic Escherichia coli. Microbiology 154: 3624–3638.
90. Fernandez-de-AlbaC, BerrowNS, Garcia-CastellanosR, GarciaJ, PonsM (2013) On the origin of the selectivity of plasmidic H-NS towards horizontally acquired DNA: linking H-NS oligomerization and cooperative DNA binding. J Mol Biol 425: 2347–2358.
91. WinardhiRS, GulvadyR, MelliesJL, YanJ (2014) Locus of Enterocyte Effacement-encoded Regulator (Ler) of Pathogenic Escherichia coli Competes Off Histone-like Nucleoid-structuring Protein (H-NS) through Noncooperative DNA Binding. J Biol Chem 289: 13739–13750.
92. LimCJ, WhangYR, KenneyLJ, YanJ (2012) Gene silencing H-NS paralogue StpA forms a rigid protein filament along DNA that blocks DNA accessibility. Nucleic Acids Res 40: 3316–3328.
93. MelliesJL, BenisonG, McNittW, MavorD, BonifaceC, et al. (2011) Ler of pathogenic Escherichia coli forms toroidal protein-DNA complexes. Microbiology 157: 1123–1133.
94. GarciaJ, CordeiroTN, PrietoMJ, PonsM (2012) Oligomerization and DNA binding of Ler, a master regulator of pathogenicity of enterohemorrhagic and enteropathogenic Escherichia coli. Nucleic Acids Res 40: 10254–10262.
95. WolfT, JanzenW, BlumC, SchnetzK (2006) Differential dependence of StpA on H-NS in autoregulation of stpA and in regulation of bgl. J Bacteriol 188: 6728–6738.
96. DatsenkoKA, WannerBL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640–6645.
97. Main-HesterKL, ColpittsKM, ThomasGA, FangFC, LibbySJ (2008) Coordinate regulation of Salmonella pathogenicity island 1 (SPI1) and SPI4 in Salmonella enterica serovar Typhimurium. Infection and immunity 76: 1024–1035.
98. AliSS, WhitneyJC, StevensonJ, RobinsonH, HowellPL, et al. (2013) Structural insights into the regulation of foreign genes in Salmonella by the Hha/H-NS complex. J Biol Chem 288: 13356–13369.
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