Adaptation and Preadaptation of to Bile
Bile possesses antibacterial activity because bile salts disrupt membranes, denature proteins, and damage DNA. This study describes mechanisms employed by the bacterium Salmonella enterica to survive bile. Sublethal concentrations of the bile salt sodium deoxycholate (DOC) adapt Salmonella to survive lethal concentrations of bile. Adaptation seems to be associated to multiple changes in gene expression, which include upregulation of the RpoS-dependent general stress response and other stress responses. The crucial role of the general stress response in adaptation to bile is supported by the observation that RpoS− mutants are bile-sensitive. While adaptation to bile involves a response by the bacterial population, individual cells can become bile-resistant without adaptation: plating of a non-adapted S. enterica culture on medium containing a lethal concentration of bile yields bile-resistant colonies at frequencies between 10−6 and 10−7 per cell and generation. Fluctuation analysis indicates that such colonies derive from bile-resistant cells present in the previous culture. A fraction of such isolates are stable, indicating that bile resistance can be acquired by mutation. Full genome sequencing of bile-resistant mutants shows that alteration of the lipopolysaccharide transport machinery is a frequent cause of mutational bile resistance. However, selection on lethal concentrations of bile also provides bile-resistant isolates that are not mutants. We propose that such isolates derive from rare cells whose physiological state permitted survival upon encountering bile. This view is supported by single cell analysis of gene expression using a microscope fluidic system: batch cultures of Salmonella contain cells that activate stress response genes in the absence of DOC. This phenomenon underscores the existence of phenotypic heterogeneity in clonal populations of bacteria and may illustrate the adaptive value of gene expression fluctuations.
Vyšlo v časopise:
Adaptation and Preadaptation of to Bile. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002459
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002459
Souhrn
Bile possesses antibacterial activity because bile salts disrupt membranes, denature proteins, and damage DNA. This study describes mechanisms employed by the bacterium Salmonella enterica to survive bile. Sublethal concentrations of the bile salt sodium deoxycholate (DOC) adapt Salmonella to survive lethal concentrations of bile. Adaptation seems to be associated to multiple changes in gene expression, which include upregulation of the RpoS-dependent general stress response and other stress responses. The crucial role of the general stress response in adaptation to bile is supported by the observation that RpoS− mutants are bile-sensitive. While adaptation to bile involves a response by the bacterial population, individual cells can become bile-resistant without adaptation: plating of a non-adapted S. enterica culture on medium containing a lethal concentration of bile yields bile-resistant colonies at frequencies between 10−6 and 10−7 per cell and generation. Fluctuation analysis indicates that such colonies derive from bile-resistant cells present in the previous culture. A fraction of such isolates are stable, indicating that bile resistance can be acquired by mutation. Full genome sequencing of bile-resistant mutants shows that alteration of the lipopolysaccharide transport machinery is a frequent cause of mutational bile resistance. However, selection on lethal concentrations of bile also provides bile-resistant isolates that are not mutants. We propose that such isolates derive from rare cells whose physiological state permitted survival upon encountering bile. This view is supported by single cell analysis of gene expression using a microscope fluidic system: batch cultures of Salmonella contain cells that activate stress response genes in the absence of DOC. This phenomenon underscores the existence of phenotypic heterogeneity in clonal populations of bacteria and may illustrate the adaptive value of gene expression fluctuations.
Zdroje
1. HofmannAF 1998 Bile secretion and enterohepatic circulation of bile acids. FeldmanMScharschmidtBFSleisengerWB Sleisenger and Fordtran's Gastrointestinal Disease, 6th ed Philadelphia, PA W. B. Saunders & Co 937 948
2. HofmannAFHageyLR 2008 Bile acids: chemistry, pathochemistry, biology, pathobiology, and therapeutics. Cell Mol Life Sci 65 2461 2483
3. BegleyMGahanCGHillC 2005 The interaction between bacteria and bile. FEMS Microbiol Rev 29 625 651
4. MerrittMEDonaldsonJR 2009 Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J Med Microbiol 58 1533 1541
5. PrietoAIRamos-MoralesFCasadesusJ 2004 Bile-induced DNA damage in Salmonella enterica. Genetics 168 1787 1794
6. PrietoAIRamos-MoralesFCasadesusJ 2006 Repair of DNA damage induced by bile salts in Salmonella enterica. Genetics 174 575 584
7. Garcia-QuintanillaMPrietoAIBarnesLRamos-MoralesFCasadesusJ 2006 Bile-induced curing of the virulence plasmid in Salmonella enterica serovar Typhimurium. J Bacteriol 188 7963 7965
8. GunnJS 2000 Mechanisms of bacterial resistance and response to bile. Microbes Infect 2 907 913
9. Andrews-PolymenisHLBaumlerAJMcCormickBAFangFC 2010 Taming the elephant: Salmonella biology, pathogenesis, and prevention. Infect Immun 78 2356 2369
10. Gonzalez-EscobedoGMarshallJMGunnJS 2011 Chronic and acute infection of the gall bladder by Salmonella Typhi: understanding the carrier state. Nat Rev Microbiol 9 9 14
11. MenendezAArenaETGuttmanJAThorsonLVallanceBA 2009 Salmonella infection of gallbladder epithelial cells drives local inflammation and injury in a model of acute typhoid fever. J Infect Dis 200 1703 1713
12. ProutyAMSchwesingerWHGunnJS 2002 Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect Immun 70 2640 2649
13. CrawfordRWRosales-ReyesRRamirez-Aguilar MdeLChapa-AzuelaOAlpuche-ArandaC 2010 Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proc Natl Acad Sci U S A 107 4353 4358
14. CasadesusJHernandezSBCotaIRamos-MoralesF 2010 Of bacteria and bile. MaloySRHughesKTCasadesusJ The Lure of Bacterial Genetics: A Tribute to John Roth Washington, D. C. ASM Press 153 162
15. PickenRNBeachamIR 1977 Bacteriophage-resistant mutants of Escherichia coli K12. Location of receptors within the lipopolysaccharide. J Gen Microbiol 102 305 318
16. MurataTTsengWGuinaTMillerSINikaidoH 2007 PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar typhimurium. J Bacteriol 189 7213 7222
17. Ramos-MoralesFPrietoAIBeuzonCRHoldenDWCasadesusJ 2003 Role for Salmonella enterica enterobacterial common antigen in bile resistance and virulence. J Bacteriol 185 5328 5332
18. ProutyAMvan VelkinburghJCGunnJS 2002 Salmonella enterica serovar Typhimurium resistance to bile: identification and characterization of the tolQRA cluster. J Bacteriol 184 1270 1276
19. PucciarelliMGPrietoAICasadesúsJGarcía-del-PortilloF 2002 Envelope instability in DNA adenine methylase mutants of Salmonella enterica. Microbiology 148 1171 1182
20. Lopez-GarridoJChengNGarcia-QuintanillaFGarcia-del PortilloFCasadesusJ 2010 Identification of the Salmonella enterica damX gene product, an inner membrane protein involved in bile resistance. J Bacteriol 192 893 895
21. ThanassiDGChengLWNikaidoH 1997 Active efflux of bile salts by Escherichia coli. J Bacteriol 179 2512 2518
22. ProutyAMBrodskyIEManosJBelasRFalkowS 2004 Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol Med Microbiol 41 177 185
23. van VelkinburghJCGunnJS 1999 PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect Immun 67 1614 1622
24. PrietoAIHernandezSBCotaIPucciarelliMGOrlovY 2009 Roles of the outer membrane protein AsmA of Salmonella enterica in the control of marRAB expression and invasion of epithelial cells. J Bacteriol 191 3615 3622
25. VeeningJWSmitsWKKuipersOP 2008 Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62 193 210
26. DavidsonCJSuretteMG 2008 Individuality in bacteria. Annu Rev Genet 42 253 268
27. ProutyAMGunnJS 2000 Salmonella enterica serovar Typhimurium invasion is repressed in the presence of bile. Infect Immun 68 6763 6769
28. MitroNGilardiFGodioCScottiEDe FabianiE 2008 Bile acids and gene regulation: from nuclear receptors to chromatin. Front Biosci 13 6276 6288
29. MariscottiJFGarcia-del PortilloF 2009 Genome expression analyses revealing the modulation of the Salmonella Rcs regulon by the attenuator IgaA. J Bacteriol 191 1855 1867
30. VijayakumarSRKirchhofMGPattenCLSchellhornHE 2004 RpoS-regulated genes of Escherichia coli identified by random lacZ fusion mutagenesis. J Bacteriol 186 8499 8507
31. HenggeR 2007 The two-component network and the general stress sigma factor RpoS (sS) in Escherichia coli. UtsumiR Bacterial Signal Transduction: Networks and Drug Targets Austin, Texas Landes Bioscience and Springer Science Business Media 40 53
32. YamanakaKZhengWCrookeEWangYHInouyeM 2001 CspD, a novel DNA replication inhibitor induced during the stationary phase in Escherichia coli. Mol Microbiol 39 1572 1584
33. YamanakaKInouyeM 1997 Growth-phase-dependent expression of cspD, encoding a member of the CspA family in Escherichia coli. J Bacteriol 179 5126 5130
34. SiegeleDA 2005 Universal stress proteins in Escherichia coli. J Bacteriol 187 6253 6254
35. RuizNKahneDSilhavyTJ 2006 Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4 57 66
36. SuvorovMLeeMHesekDBoggessBMobasheryS 2008 Lytic transglycosylase MltB of Escherichia coli and its role in recycling of peptidoglycan strands of bacterial cell wall. J Am Chem Soc 130 11878 11879
37. PrietoAIHernándezSBCotaIPucciarelliMGOrlovY 2009 Roles of the outer membrane protein AsmA of Salmonella enterica in control of marRAB expression and invasion of epithelial cells. J Bacteriol 191 3615 3622
38. PiddockLJ 2006 Multidrug-resistance efflux pumps - not just for resistance. Nat Rev Microbiol 4 629 636
39. ProutyAMBrodskyIEManosJBelasRFalkowS 2004 Transcriptional regulation fo Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol Med Microbiol 41 177 185
40. PapezovaKGregorovaDJonuschiesJRychlikI 2007 Ordered expression of virulence genes in Salmonella enterica serovar Typhimurium. Folia Microbiol (Praha) 52 107 114
41. NishinoKLatifiTGroismanEA 2006 Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol Microbiol 59 126 141
42. LuriaSEDelbruckM 1943 Mutations of bacteria from virus sensitivity to virus Resistance. Genetics 28 491 511
43. MardisER 2008 Next-generation DNA sequencing methods. Annu Rev Genomics Hum Genet 9 387 402
44. ChngSSRuizNChimalakondaGSilhavyTJKahneD 2010 Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc Natl Acad Sci U S A 107 5363 5368
45. WuTMcCandlishACGronenbergLSChngSSSilhavyTJ 2006 Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci U S A 103 11754 11759
46. TooneWMRuddKEFriesenJD 1991 deaD, a new Escherichia coli gene encoding a presumed ATP-dependent RNA helicase, can suppress a mutation in rpsB, the gene encoding ribosomal protein S2. J Bacteriol 173 3291 3302
47. RuizNKahneDSilhavyTJ 2009 Transport of lipopolysaccharide across the cell envelope: the long road of discovery. Nat Rev Microbiol 7 677 683
48. SperandeoPDehoGPolissiA 2009 The lipopolysaccharide transport system of Gram-negative bacteria. Biochim Biophys Acta 1791 594 602
49. SperandeoPLauFKCarpentieriADe CastroCMolinaroA 2008 Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190 4460 4469
50. DucretAMaisonneuveENotareschiPGrossiAMignotT 2009 A microscope automated fluidic system to study bacterial processes in real time. PLoS ONE 4 e7282 doi:10.1371/journal.pone.0007282
51. DrakeJWCharlesworthBCharlesworthDCrowJF 1998 Rates of spontaneous mutation. Genetics 148 1667 1686
52. CasadesusJLowD 2006 Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 70 830 856
53. SatoryDGordonAJHallidayJAHermanC 2011 Epigenetic switches: can infidelity govern fate in microbes? Curr Opin Microbiol 14 212 217
54. Jimenez-SanchezACerda-OlmedoE 1975 Mutation and DNA replication in Escherichia coli treated with low concentrations of N-methyl-N′-nitro-N-nitrosoguanidine. Mutat Res 28 337 345
55. SchmiegerH 1972 Phage P22 mutants with increased or decreased transducing abilities. Mol Gen Genet 119 75 88
56. GarzonACanoDACasadesusJ 1995 Role of Erf recombinase in P22-mediated plasmid transduction. Genetics 140 427 434
57. ChanRKBotsteinDWatanabeTOgataY 1972 Specialized transduction of tetracycline by phage P22 in Salmonella typhimurium. II. Properties of a high frequency transducing lysate. Virology 50 883 898
58. VogelHBonnerD 1956 Acetylornithase of Escherichia coli: partial purification and some properties. J Biol Chem 218 97 106
59. DatsenkoKAWannerBL 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 90 6640 6645
60. EllermeierCDJanakiramASlauchJM 2002 Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. Gene 290 153 161
61. HautefortIProencaMJHintonJC 2003 Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl Environ Microbiol 69 7480 7491
62. WuTT 1966 A model for three-point analysis of random general transduction. Genetics 54 405 410
63. FullwoodMJWeiCLLiuETRuanY 2009 Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res 19 521 532
64. ManganMWLucchiniSDaninoVCroininTOHintonJC 2006 The integration host factor (IHF) integrates stationary-phase and virulence gene expression in Salmonella enterica serovar Typhimurium. Mol Microbiol 59 1831 1847
65. SmythGKSpeedT 2003 Normalization of cDNA microarray data. Methods 31 265 273
66. MillerJH 1972 Experiments in Molecular Genetics Cold Spring Harbor, N. Y. Cold Spring Harbor Laboratory Press
67. Buendia-ClaveriaAMMoussaidAOlleroFJVinardellJMTorresA 2003 A purL mutant of Sinorhizobium fredii HH103 is symbiotically defective and altered in its lipopolysaccharide. Microbiology 149 1807 1818
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 1
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Microenvironmental Regulation by Fibrillin-1
- Poly(ADP-Ribose) Polymerase 1 (PARP-1) Regulates Ribosomal Biogenesis in Nucleoli
- Parallel Mapping and Simultaneous Sequencing Reveals Deletions in and Associated with Discrete Inherited Disorders in a Domestic Dog Breed
- Two-Component Elements Mediate Interactions between Cytokinin and Salicylic Acid in Plant Immunity