全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS Genetics  2015 

Epigenetic Control of Salmonella enterica O-Antigen Chain Length: A Tradeoff between Virulence and Bacteriophage Resistance

DOI: 10.1371/journal.pgen.1005667

Full-Text   Cite this paper   Add to My Lib

Abstract:

The Salmonella enterica opvAB operon is a horizontally-acquired locus that undergoes phase variation under Dam methylation control. The OpvA and OpvB proteins form intertwining ribbons in the inner membrane. Synthesis of OpvA and OpvB alters lipopolysaccharide O-antigen chain length and confers resistance to bacteriophages 9NA (Siphoviridae), Det7 (Myoviridae), and P22 (Podoviridae). These phages use the O-antigen as receptor. Because opvAB undergoes phase variation, S. enterica cultures contain subpopulations of opvABOFF and opvABON cells. In the presence of a bacteriophage that uses the O-antigen as receptor, the opvABOFF subpopulation is killed and the opvABON subpopulation is selected. Acquisition of phage resistance by phase variation of O-antigen chain length requires a payoff: opvAB expression reduces Salmonella virulence. However, phase variation permits resuscitation of the opvABOFF subpopulation as soon as phage challenge ceases. Phenotypic heterogeneity generated by opvAB phase variation thus preadapts Salmonella to survive phage challenge with a fitness cost that is transient only.

References

[1]  Shapiro L (1976) Differentiation in the Caulobacter cell cycle. Annu Rev Microbiol 30: 377–407. pmid:185940 doi: 10.1146/annurev.mi.30.100176.002113
[2]  Kaiser D (1986) Control of multicellular development: Dictyostelium and Myxococcus. Annu Rev Genet 20: 539–566. pmid:3028248 doi: 10.1146/annurev.ge.20.120186.002543
[3]  Stragier P, Losick R (1996) Molecular genetics of sporulation in Bacillus subtilis. Annu Rev Genet 30: 297–241. pmid:8982457 doi: 10.1146/annurev.genet.30.1.297
[4]  Andrewes FW (1922) Studies in group agglutination. I. The Salmonella group and its antigenic structure. J Path Bact 25: 505–524. doi: 10.1002/path.1700250411
[5]  Legroux R, Magrou J (1920) état organisé des colonies bactériennes. Ann Inst Pasteur (Paris) 34: 417–431.
[6]  Shapiro JA, Higgins NP (1989) Differential activity of a transposable element in Escherichia coli colonies. J Bacteriol 171: 5975–5986. pmid:2553666
[7]  Shapiro JA (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52: 81–104. pmid:9891794 doi: 10.1146/annurev.micro.52.1.81
[8]  Zgur-Bertok D (2007) Phenotypic heterogeneity in bacterial populations. Acta Agric Slovenica 90: 17–24.
[9]  Dhar N, McKinney JD (2007) Microbial phenotypic heterogeneity and antibiotic tolerance. Curr Opin Microbiol 10: 30–38. pmid:17215163 doi: 10.1016/j.mib.2006.12.007
[10]  Davidson CJ, Surette MG (2008) Individuality in bacteria. Annu Rev Genet 42: 253–268. doi: 10.1146/annurev.genet.42.110807.091601. pmid:18652543
[11]  Veening JW, Smits WK, Kuipers OP (2008) Bistability, epigenetics, and bet-hedging in bacteria. Annu Rev Microbiol 62: 193–210. doi: 10.1146/annurev.micro.62.081307.163002. pmid:18537474
[12]  Casadesus J, Low DA (2013) Programmed heterogeneity: epigenetic mechanisms in bacteria. J Biol Chem 288: 13929–13935. doi: 10.1074/jbc.R113.472274. pmid:23592777
[13]  Thattai M, van Oudenaarden A (2004) Stochastic gene expression in fluctuating environments. Genetics 167: 523–530. pmid:15166174 doi: 10.1534/genetics.167.1.523
[14]  Kussell E, Leibler S (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075–2078. pmid:16123265 doi: 10.1126/science.1114383
[15]  Wolf DM, Vazirani VV, Arkin AP (2005) Diversity in times of adversity: probabilistic strategies in microbial survival games. J Theor Biol 234: 227–253. pmid:15757681 doi: 10.1016/j.jtbi.2004.11.020
[16]  Hernandez SB, Cota I, Ducret A, Aussel L, Casadesus J (2012) Adaptation and preadaptation of Salmonella enterica to bile. PLoS Genet 8: e1002459. doi: 10.1371/journal.pgen.1002459. pmid:22275872
[17]  Sanchez-Romero MA, Casadesus J (2014) Contribution of phenotypic heterogeneity to adaptive antibiotic resistance. Proc Natl Acad Sci U S A 111: 355–360. doi: 10.1073/pnas.1316084111. pmid:24351930
[18]  Ni M, Decrulle AL, Fontaine F, Demarez A, Taddei F, et al. (2012) Pre-disposition and epigenetics govern variation in bacterial survival upon stress. PLoS Genet 8: e1003148. doi: 10.1371/journal.pgen.1003148. pmid:23284305
[19]  Silverman M, Zieg J, Hilmen M, Simon M (1979) Phase variation in Salmonella: genetic analysis of a recombinational switch. Proc Natl Acad Sci U S A 76: 391–395. pmid:370828 doi: 10.1073/pnas.76.1.391
[20]  Moxon ER, Rainey PB, Nowak MA, Lenski RE (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4: 24–33. pmid:7922307 doi: 10.1016/s0960-9822(00)00005-1
[21]  Moxon R, Bayliss C, Hood D (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40: 307–333. pmid:17094739 doi: 10.1146/annurev.genet.40.110405.090442
[22]  Dubnau D, Losick R (2006) Bistability in bacteria. Mol Microbiol 61: 564–572. pmid:16879639 doi: 10.1111/j.1365-2958.2006.05249.x
[23]  Hernday A, Krabbe M, Braaten B, Low D (2002) Self-perpetuating epigenetic pili switches in bacteria. Proc Natl Acad Sci U S A 99: 16470–16476. pmid:12202745 doi: 10.1073/pnas.182427199
[24]  Casadesus J, Low D (2006) Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 70: 830–856. pmid:16959970 doi: 10.1128/mmbr.00016-06
[25]  van der Woude MW (2011) Phase variation: how to create and coordinate population diversity. Curr Opin Microbiol 14: 205–211. doi: 10.1016/j.mib.2011.01.002. pmid:21292543
[26]  van der Woude MW, Baumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17: 581–611, table of contents. pmid:15258095 doi: 10.1128/cmr.17.3.581-611.2004
[27]  van der Woude MW (2006) Re-examining the role and random nature of phase variation. FEMS Microbiol Lett 254: 190–197. pmid:16445745 doi: 10.1111/j.1574-6968.2005.00038.x
[28]  Kim M, Ryu S (2012) Spontaneous and transient defence against bacteriophage by phase-variable glucosylation of O-antigen in Salmonella enterica serovar Typhimurium. Mol Microbiol 86: 411–425. doi: 10.1111/j.1365-2958.2012.08202.x. pmid:22928771
[29]  Zaleski P, Wojciechowski M, Piekarowicz A (2005) The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection. Microbiology 151: 3361–3369. pmid:16207918 doi: 10.1099/mic.0.28184-0
[30]  Srikhanta YN, Maguire TL, Stacey KJ, Grimmond SM, Jennings MP (2005) The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc Natl Acad Sci U S A 102: 5547–5551. pmid:15802471 doi: 10.1073/pnas.0501169102
[31]  Hoskisson PA, Smith MC (2007) Hypervariation and phase variation in the bacteriophage 'resistome'. Curr Opin Microbiol 10: 396–400. pmid:17719266 doi: 10.1016/j.mib.2007.04.003
[32]  Cota I, Blanc-Potard AB, Casadesus J (2012) STM2209-STM2208 (opvAB): a phase variation locus of Salmonella enterica involved in control of O-antigen chain length. PLoS One 7: e36863. doi: 10.1371/journal.pone.0036863. pmid:22606300
[33]  Ghosh AS, Young KD (2005) Helical disposition of proteins and lipopolysaccharide in the outer membrane of Escherichia coli. J Bacteriol 187: 1913–1922. pmid:15743937 doi: 10.1128/jb.187.6.1913-1922.2005
[34]  Murray GL, Attridge SR, Morona R (2003) Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz. Mol Microbiol 47: 1395–1406. pmid:12603743 doi: 10.1046/j.1365-2958.2003.03383.x
[35]  Goldman RC, Hunt F (1990) Mechanism of O-antigen distribution in lipopolysaccharide. J Bacteriol 172: 5352–5359. pmid:1697578
[36]  Bastin DA, Stevenson G, Brown PK, Haase A, Reeves PR (1993) Repeat unit polysaccharides of bacteria: a model for polymerization resembling that of ribosomes and fatty acid synthetase, with a novel mechanism for determining chain length. Mol Microbiol 7: 725–734. pmid:7682279 doi: 10.1111/j.1365-2958.1993.tb01163.x
[37]  Daniels C, Morona R (1999) Analysis of Shigella flexneri Wzz (Rol) function by mutagenesis and cross-linking: Wzz is able to oligomerize. Mol Microbiol 34: 181–194. pmid:10540296 doi: 10.1046/j.1365-2958.1999.01591.x
[38]  Batchelor RA, Alifano P, Biffali E, Hull SI, Hull RA (1992) Nucleotide sequences of the genes regulating O-polysaccharide antigen chain length (rol) from Escherichia coli and Salmonella typhimurium: protein homology and functional complementation. J Bacteriol 174: 5228–5236. pmid:1379582
[39]  Lindberg AA (1973) Bacteriophage receptors. Annu Rev Microbiol 27: 205–241. pmid:4584686 doi: 10.1146/annurev.mi.27.100173.001225
[40]  Kintz E, Davies MR, Hammarlof DL, Canals R, Hinton JC, et al. (2015) A BTP1 prophage gene present in invasive non-typhoidal Salmonella determines composition and length of the O-antigen of the lipopolysaccharide. Mol Microbiol 96: 263–275. doi: 10.1111/mmi.12933. pmid:25586744
[41]  Wilkinson RG, Gemski P Jr., Stocker BA (1972) Non-smooth mutants of Salmonella typhimurium: differentiation by phage sensitivity and genetic mapping. J Gen Microbiol 70: 527–554. pmid:4556257 doi: 10.1099/00221287-70-3-527
[42]  Casjens SR, Leavitt JC, Hatfull GF, Hendrix RW (2014) Genome sequence of Salmonella phage 9NA. Genome Announc 2: e00531–14 doi: 10.1128/genomeA.00531-14. pmid:25146133
[43]  Walter M, Fiedler C, Grassl R, Biebl M, Rachel R, et al. (2008) Structure of the receptor-binding protein of bacteriophage det7: a podoviral tail spike in a myovirus. J Virol 82: 2265–2273. pmid:18077713 doi: 10.1128/jvi.01641-07
[44]  Casjens SR, Jacobs-Sera D, Hatfull GF, Hendrix RW (2015) Genome sequence of Salmonella enterica phage Det7. Genome Announc 3: e00279–00215. doi: 10.1128/genomeA.00279-15. pmid:25953168
[45]  Smith HO, Levine M (1964) Two sequential repressions of DNA synthesis in the establishment of lysogeny by phage P22 and Its mutants. Proc Natl Acad Sci U S A 52: 356–363. pmid:14206603 doi: 10.1073/pnas.52.2.356
[46]  Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635–700. pmid:12045108 doi: 10.1146/annurev.biochem.71.110601.135414
[47]  Bravo D, Silva C, Carter JA, Hoare A, Alvarez SA, et al. (2008) Growth-phase regulation of lipopolysaccharide O-antigen chain length influences serum resistance in serovars of Salmonella. J Med Microbiol 57: 938–946. doi: 10.1099/jmm.0.47848-0. pmid:18628492
[48]  Beuzon CR, Holden DW (2001) Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect 3: 1345–1352. pmid:11755424 doi: 10.1016/s1286-4579(01)01496-4
[49]  Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am Nat 100: 687–690. doi: 10.1086/282461
[50]  Nystrom T (2004) Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol Microbiol 54: 855–862. pmid:15522072 doi: 10.1111/j.1365-2958.2004.04342.x
[51]  Shoval O, Sheftel H, Shinar G, Hart Y, Ramote O, et al. (2012) Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space. Science 336: 1157–1160. doi: 10.1126/science.1217405. pmid:22539553
[52]  Bailly-Bechet M, Benecke A, Hardt WD, Lanza V, Sturm A, et al. (2011) An externally modulated, noise-driven switch for the regulation of SPI1 in Salmonella enterica serovar Typhimurium. J Math Biol 63: 637–662. doi: 10.1007/s00285-010-0385-1. pmid:21107576
[53]  Ferenci T, Spira B (2007) Variation in stress responses within a bacterial species and the indirect costs of stress resistance. Ann N Y Acad Sci 1113: 105–113. pmid:17483210 doi: 10.1196/annals.1391.003
[54]  Andersson DI, Hughes D (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 8: 260–271. doi: 10.1038/nrmicro2319. pmid:20208551
[55]  De Paepe M, Gaboriau-Routhiau V, Rainteau D, Rakotobe S, Taddei F, et al. (2011) Trade-off between bile resistance and nutritional competence drives Escherichia coli diversification in the mouse gut. PLoS Genet 7: e1002107. doi: 10.1371/journal.pgen.1002107. pmid:21698140
[56]  Vincent BM, Lancaster AK, Scherz-Shouval R, Whitesell L, Lindquist S (2013) Fitness trade-offs restrict the evolution of resistance to amphotericin B. PLoS Biol 11: e1001692. doi: 10.1371/journal.pbio.1001692. pmid:24204207
[57]  Leon M, Bastias R (2015) Virulence reduction in bacteriophage resistant bacteria. Front Microbiol 6: 343. doi: 10.3389/fmicb.2015.00343. pmid:25954266
[58]  Taylor VL, Udaskin ML, Islam ST, Lam JS (2013) The D3 bacteriophage alpha-polymerase inhibitor (Iap) peptide disrupts O-antigen biosynthesis through mimicry of the chain length regulator Wzz in Pseudomonas aeruginosa. J Bacteriol 195: 4735–4741. doi: 10.1128/JB.00903-13. pmid:23955007
[59]  Susskind MM, Botstein D (1978) Molecular genetics of bacteriophage P22. Microbiol Rev 42: 385–413. pmid:353481
[60]  Whitfield C, Trent MS (2014) Biosynthesis and export of bacterial lipopolysaccharides. Annu Rev Biochem 83: 99–128. doi: 10.1146/annurev-biochem-060713-035600. pmid:24580642
[61]  Wilson GG, Murray NE (1991) Restriction and modification systems. Annu Rev Genet 25: 585–627. pmid:1812816 doi: 10.1146/annurev.ge.25.120191.003101
[62]  Lee DJ, Bingle LE, Heurlier K, Pallen MJ, Penn CW, et al. (2009) Gene doctoring: a method for recombineering in laboratory and pathogenic Escherichia coli strains. BMC Microbiol 9: 252. doi: 10.1186/1471-2180-9-252. pmid:20003185
[63]  Datsenko KA, Wanner BL (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. pmid:10829079 doi: 10.1073/pnas.120163297
[64]  Hautefort I, Proenca MJ, Hinton JC (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. pmid:14660401 doi: 10.1128/aem.69.12.7480-7491.2003
[65]  Chan RK, Botstein D, Watanabe T, Ogata Y (1972) Specialized transduction of tetracycline by phage P22 in Salmonella typhimurium. II. Properties of a high frequency transducing lysate. Virology 50: 883–898. pmid:4565618 doi: 10.1016/0042-6822(72)90442-4
[66]  Torreblanca J, Casadesús J (1996) DNA adenine methylase mutants of Salmonella typhimurium and a novel Dam-regulated locus. Genetics 144: 15–26. pmid:8878670
[67]  Buendia-Claveria AM, Moussaid A, Ollero FJ, Vinardell JM, Torres A, et al. (2003) A purL mutant of Sinorhizobium fredii HH103 is symbiotically defective and altered in its lipopolysaccharide. Microbiology 149: 1807–1818. pmid:12855732 doi: 10.1099/mic.0.26099-0
[68]  Segura I, Casadesus J, Ramos-Morales F (2004) Use of mixed infections to study cell invasion and intracellular proliferation of Salmonella enterica in eukaryotic cell cultures. J Microbiol Methods 56: 83–91. pmid:14706753 doi: 10.1016/j.mimet.2003.09.004

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133