A long-term epigenetic memory switch controls bacterial virulence bimodality

eLife

Volumn 6, Issue , 2017, Pages

  Ronin, Irine ^a   Katsowich, Naama ^b   Rosenshine, Ilan ^b   Balaban, Nathalie Q ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

GENTAMICIN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BIMODAL GROWTH; CELL ADHESION ASSAY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENTEROPATHOGENIC ESCHERICHIA COLI; EPIGENETIC MEMORY; EPIGENETICS; FLUORESCENCE ACTIVATED CELL SORTING; GENE ACTIVITY; GENE INACTIVATION; GENE SWITCHING; GENETIC REGULATION; IMMUNOHISTOCHEMISTRY; MATHEMATICAL ANALYSIS; MORPHOTYPE; NONHUMAN; OPERON; PERSISTENT INFECTION; PHASE CONTRAST MICROSCOPY; WESTERN BLOTTING; WHOLE GENOME SEQUENCING; ESCHERICHIA COLI; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; THEORETICAL MODEL; VIRULENCE;

EPIGENESIS, GENETIC; ESCHERICHIA COLI; MODELS, THEORETICAL; VIRULENCE; VIRULENCE FACTORS;

EID: 85011954441     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.19599     Document Type: Article

References (69)

1. Ackermann M, Stecher B, Freed NE, Songhet P, Hardt WD, Doebeli M. 2008. Self-destructive cooperation mediated by phenotypic noise. Nature 454:987-990.doi: 10.1038/nature07067, PMID: 18719588.
2. Arnoldini M, Vizcarra IA, Peña-Miller R, Stocker N, Diard M, Vogel V, Beardmore RE, Hardt WD, Ackermann M. 2014. Bistable expression of virulence genes in salmonella leads to the formation of an antibiotic-tolerant subpopulation. PLoS Biology 12:e1001928.doi: 10.1371/journal.pbio.1001928, PMID: 25136970.
3. Atack JM, Srikhanta YN, Fox KL, Jurcisek JA, Brockman KL, Clark TA, Boitano M, Power PM, Jen FE, McEwan AG, Grimmond SM, Smith AL, Barenkamp SJ, Korlach J, Bakaletz LO, Jennings MP. 2015. A biphasic epigenetic switch controls immunoevasion, virulence and niche adaptation in non-typeable Haemophilus influenzae. Nature Communications 6:7828.doi: 10.1038/ncomms8828, PMID: 26215614.
4. Avery SV. 2006. Microbial cell individuality and the underlying sources of heterogeneity. Nature Reviews Microbiology 4:577-587.doi: 10.1038/nrmicro1460, PMID: 16845428.
5. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. 2004. Bacterial persistence as a phenotypic switch. Science 305:1622-1625.doi: 10.1126/science.1099390, PMID: 15308767.
6. Baldini MM, Kaper JB, Levine MM, Candy DC, Moon HW. 1983. Plasmid-mediated adhesion in Enteropathogenic Escherichia coli. Journal of Pediatric Gastroenterology and Nutrition 2:534-538.doi: 10.1097/00005176-198302030-00023, PMID: 6352891.
7. Benjamin P, Federman M, Wanke CA. 1995. Characterization of an invasive phenotype associated with enteroaggregative escherichia coli. Infection and Immunity 63:3417-3421. PMID: 7642271.
8. Berdichevsky T, Friedberg D, Nadler C, Rokney A, Oppenheim A, Rosenshine I. 2005. Ler is a negative autoregulator of the LEE1 operon in Enteropathogenic Escherichia coli. Journal of Bacteriology 187:349-357.doi: 10.1128/JB.187.1.349-357.2005, PMID: 15601719.
9. Bieber D, Ramer SW, Wu CY, Murray WJ, Tobe T, Fernandez R, Schoolnik GK. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:2114-2118.doi: 10.1126/science.280.5372.2114, PMID: 9641917.
10. Brauner A, Fridman O, Gefen O, Balaban NQ. 2016. Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nature Reviews Microbiology 14:320-330.doi: 10.1038/nrmicro.2016.34, PMID: 27080241.
11. Bustamante VH, Villalba MI, García-Angulo VA, Vázquez A, Martínez LC, Jiménez R, Puente JL. 2011. PerC and GrlA independently regulate Ler expression in Enteropathogenic Escherichia coli. Molecular Microbiology 82: 398-415.doi: 10.1111/j.1365-2958.2011.07819.x, PMID: 21895790.
12. Casadesús J, Low DA. 2013. Programmed heterogeneity: epigenetic mechanisms in bacteria. Journal of Biological Chemistry 288:13929-13935.doi: 10.1074/jbc.R113.472274, PMID: 23592777.
13. Clarke SC, Haigh RD, Freestone PP, Williams PH. 2003. Virulence of Enteropathogenic Escherichia Coli, a global pathogen. Clinical Microbiology Reviews 16:365-378.doi: 10.1128/CMR.16.3.365-378.2003, PMID: 12857773.
14. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in escherichia coli K-12 using PCR products. PNAS 97:6640-6645.doi: 10.1073/pnas.120163297, PMID: 10829079.
15. De Angelis G, Moschioni M, Muzzi A, Pezzicoli A, Censini S, Delany I, Lo Sapio M, Sinisi A, Donati C, Masignani V, Barocchi MA. 2011. The Streptococcus pneumoniae pilus-1 displays a biphasic expression pattern. PLoS One 6:e21269.doi: 10.1371/journal.pone.0021269, PMID: 21731688.
16. Deris JB, Kim M, Zhang Z, Okano H, Hermsen R, Groisman A, Hwa T. 2013. The innate growth bistability and fitness landscapes of antibiotic-resistant bacteria. Science 342:1237435.doi: 10.1126/science.1237435, PMID: 24288338.
17. Diard M, Garcia V, Maier L, Remus-Emsermann MN, Regoes RR, Ackermann M, Hardt WD. 2013. Stabilization of cooperative virulence by the expression of an avirulent phenotype. Nature 494:353-356.doi: 10.1038/nature11913, PMID: 23426324.
18. Donnenberg MS, Girón JA, Nataro JP, Kaper JB. 1992. A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Molecular Microbiology 6:3427-3437.doi: 10.1111/j.1365-2958.1992.tb02210.x, PMID: 1362446.
19. Dubnau D, Losick R. 2006. Bistability in bacteria. Molecular Microbiology 61:564-572.doi: 10.1111/j.1365-2958.2006.05249.x, PMID: 16879639.
20. Fraser D, Kaern M. 2009. A chance at survival: gene expression noise and phenotypic diversification strategies. Molecular Microbiology 71:1333-1340.doi: 10.1111/j.1365-2958.2009.06605.x, PMID: 19220745.
21. Friedberg D, Umanski T, Fang Y, Rosenshine I. 1999. Hierarchy in the expression of the locus of enterocyte effacement genes of enteropathogenic Escherichia coli. Molecular Microbiology 34:941-952.doi: 10.1046/j.1365-2958.1999.01655.x, PMID: 10594820.
22. Gaytán MO, Martínez-Santos VI, Soto E, González-Pedrajo B. 2016. Type three Secretion System in attaching and effacing Pathogens. Frontiers in Cellular and Infection Microbiology 6:129.doi: 10.3389/fcimb.2016.00129, PMID: 27818950.
23. Gefen O, Gabay C, Mumcuoglu M, Engel G, Balaban NQ. 2008. Single-cell protein induction dynamics reveals a period of vulnerability to antibiotics in persister bacteria. PNAS 105:6145-6149.doi: 10.1073/pnas.0711712105, PMID: 18427112.
24. Girón JA, Torres AG, Freer E, Kaper JB. 2002. The flagella of enteropathogenic Escherichia Coli mediate adherence to epithelial cells. Molecular Microbiology 44:361-379.doi: 10.1046/j.1365-2958.2002.02899.x, PMID: 11972776.
25. Goldberg A, Fridman O, Ronin I, Balaban NQ. 2014. Systematic identification and quantification of phase variation in commensal and pathogenic Escherichia coli. Genome Medicine 6:112.doi: 10.1186/s13073-014-0112-4, PMID: 25530806.
26. Gómez-Duarte OG, Kaper JB. 1995. A plasmid-encoded regulatory region activates chromosomal eaeA expression in Enteropathogenic Escherichia coli. Infection and Immunity 63:1767-1776. PMID: 7729884.
27. Hautefort I, Proença 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. Applied and Environmental Microbiology 69:7480-7491.doi: 10.1128/AEM.69.12.7480-7491.2003, PMID: 14660401.
28. Hazen TH, Daugherty SC, Shetty A, Mahurkar AA, White O, Kaper JB, Rasko DA. 2015a. RNA-Seq analysis of isolate-and growth phase-specific differences in the global transcriptomes of enteropathogenic Escherichia coli prototype isolates. Frontiers in Microbiology 6:569.doi: 10.3389/fmicb.2015.00569, PMID: 26124752.
29. Hazen TH, Donnenberg MS, Panchalingam S, Antonio M, Hossain A, Mandomando I, Ochieng JB, Ramamurthy T, Tamboura B, Qureshi S, Quadri F, Zaidi A, Kotloff KL, Levine MM, Barry EM, Kaper JB, Rasko DA, Nataro JP. 2016. Genomic diversity of EPEC associated with clinical presentations of differing severity. Nature Microbiology 1:15014.doi: 10.1038/nmicrobiol.2015.14, PMID: 27571975.
30. Hazen TH, Kaper JB, Nataro JP, Rasko DA. 2015b. Comparative genomics provides insight into the diversity of the attaching and effacing escherichia coli virulence plasmids. Infection and Immunity 83:4103-4117.doi: 10.1128/IAI.00769-15, PMID: 26238712.
31. Helaine S, Holden DW. 2013. Heterogeneity of intracellular replication of bacterial pathogens. Current Opinion in Microbiology 16:184-191.doi: 10.1016/j.mib.2012.12.004, PMID: 23485258.
32. Ibarra JA, Villalba MI, Puente JL. 2003. Identification of the DNA binding sites of PerA, the transcriptional activator of the bfp and per operons in enteropathogenic Escherichia coli. Journal of Bacteriology 185:2835-2847.doi: 10.1128/JB.185.9.2835-2847.2003, PMID: 12700263.
33. Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, Henderson IR, Harris D, Asadulghani M, Kurokawa K, Dean P, Kenny B, Quail MA, Thurston S, Dougan G, Hayashi T, Parkhill J, Frankel G. 2009. Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. Journal of Bacteriology 191:347-354.doi: 10.1128/JB.01238-08, PMID: 18952797.
34. Ingle DJ, Tauschek M, Edwards DJ, Hocking DM, Pickard DJ, Azzopardi KI, Amarasena T, Bennett-Wood V, Pearson JS, Tamboura B, Antonio M, Ochieng JB, Oundo J, Mandomando I, Qureshi S, Ramamurthy T, Hossain A, Kotloff KL, Nataro JP, Dougan G, et al. 2016. Evolution of atypical enteropathogenic E. coli by repeated acquisition of LEE pathogenicity island variants. Nature Microbiology 1:15010.doi: 10.1038/nmicrobiol.2015.10, PMID: 27571974.
35. Irwin PL, Nguyen LH, Paoli GC, Chen CY. 2010. Evidence for a bimodal distribution of Escherichia coli doubling times below a threshold initial cell concentration. BMC microbiology 10:207.doi: 10.1186/1471-2180-10-207, PMID: 20678197.
36. Iyoda S, Koizumi N, Satou H, Lu Y, Saitoh T, Ohnishi M, Watanabe H. 2006. The GrlR-GrlA regulatory system coordinately controls the expression of flagellar and LEE-encoded type III protein secretion systems in Enterohemorrhagic Escherichia coli. Journal of Bacteriology 188:5682-5692.doi: 10.1128/JB.00352-06, PMID: 16885436.
37. Kamada N, Sakamoto K, Seo SU, Zeng MY, Kim YG, Cascalho M, Vallance BA, Puente JL, Núñez G. 2015. Humoral Immunity in the Gut selectively targets phenotypically virulent Attaching-and-Effacing Bacteria for intraluminal Elimination. Cell Host & Microbe 17:617-627.doi: 10.1016/j.chom.2015.04.001, PMID: 25936799.
38. Kenny B, Abe A, Stein M, Finlay BB. 1997. Enteropathogenic Escherichia Coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infection and Immunity 65:2606-2612. PMID: 9199427.
39. Kussell E, Leibler S. 2005. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309:2075-2078.doi: 10.1126/science.1114383, PMID: 16123265.
40. Leverton LQ, Kaper JB. 2005. Temporal expression of enteropathogenic Escherichia coli virulence genes in an in vitro model of infection. Infection and Immunity 73:1034-1043.doi: 10.1128/IAI.73.2.1034-1043.2005, PMID: 15664947.
41. Levin-Reisman I, Gefen O, Fridman O, Ronin I, Shwa D, Sheftel H, Balaban NQ. 2010. Automated imaging with ScanLag reveals previously undetectable bacterial growth phenotypes. Nature Methods 7:737-739.doi: 10.1038/nmeth.1485, PMID: 20676109.
42. Levine JH, Fontes ME, Dworkin J, Elowitz MB. 2012. Pulsed feedback defers cellular differentiation. PLoS Biology 10:e1001252.doi: 10.1371/journal.pbio.1001252, PMID: 22303282.
43. Levine MM, Bergquist EJ, Nalin DR, Waterman DH, Hornick RB, Young CR, Sotman S. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1:1119-1122.doi: 10.1016/S0140-6736(78)90299-4, PMID: 77415.
44. Lewis K. 2000. Programmed death in bacteria. Microbiology and Molecular Biology Reviews 64:503-514.doi: 10.1128/MMBR.64.3.503-514.2000, PMID: 10974124.
45. Lutz R, Bujard H. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/ O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Research 25:1203-1210.doi: 10.1093/nar/25.6.1203, PMID: 9092630.
46. Martínez-Laguna Y, Calva E, Puente JL. 1999. Autoactivation and environmental regulation of bfpT expression, the gene coding for the transcriptional activator of bfpA in enteropathogenic Escherichia coli. Molecular Microbiology 33:153-166.doi: 10.1046/j.1365-2958.1999.01460.x, PMID: 10411732.
47. McClain MS, Blomfield IC, Eisenstein BI. 1991. Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1. Fimbriae in Escherichia coli. Journal of Bacteriology 173:5308-5314.doi: 10.1128/jb.173.17.5308-5314.1991, PMID: 1679430.
48. Mellies JL, Barron AM, Carmona AM. 2007. Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infection and Immunity 75:4199-4210.doi: 10.1128/IAI.01927-06, PMID: 17576759.
49. Mitrophanov AY, Groisman EA. 2008. Positive feedback in cellular control systems. BioEssays 30:542-555.doi: 10.1002/bies.20769, PMID: 18478531.
50. Nielsen AT, Dolganov NA, Rasmussen T, Otto G, Miller MC, Felt SA, Torreilles S, Schoolnik GK. 2010. A bistable switch and anatomical site control Vibrio cholerae virulence gene expression in the intestine. PLoS Pathogens 6:e1001102.doi: 10.1371/journal.ppat.1001102, PMID: 20862321.
51. Ozbudak EM, Thattai M, Lim HN, Shraiman BI, Van Oudenaarden A. 2004. Multistability in the lactose utilization network of Escherichia coli. Nature 427:737-740.doi: 10.1038/nature02298, PMID: 14973486.
52. Padavannil A, Jobichen C, Mills E, Velazquez-Campoy A, Li M, Leung KY, Mok YK, Rosenshine I, Sivaraman J. 2013. Structure of GrlR-GrlA complex that prevents GrlA activation of virulence genes. Nature Communications 4:2546.doi: 10.1038/ncomms3546, PMID: 24092262.
53. Porter ME, Mitchell P, Roe AJ, Free A, Smith DG, Gally DL. 2004. Direct and indirect transcriptional activation of virulence genes by an AraC-like protein, PerA from enteropathogenic Escherichia coli. Molecular Microbiology 54:1117-1133.doi: 10.1111/j.1365-2958.2004.04333.x, PMID: 15522091.
54. Puente JL, Bieber D, Ramer SW, Murray W, Schoolnik GK. 1996. The bundle-forming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals. Molecular Microbiology 20:87-100.doi: 10.1111/j.1365-2958.1996.tb02491.x, PMID: 8861207.
55. Roe AJ, Naylor SW, Spears KJ, Yull HM, Dransfield TA, Oxford M, McKendrick IJ, Porter M, Woodward MJ, Smith DG, Gally DL. 2004. Co-ordinate single-cell expression of LEE4-and LEE5-encoded proteins of Escherichia coli O157:H7. Molecular Microbiology 54:337-352.doi: 10.1111/j.1365-2958.2004.04277.x, PMID: 15469507.
56. Rosenshine I, Ruschkowski S, Finlay BB. 1996. Expression of attaching/effacing activity by enteropathogenic Escherichia coli depends on growth phase, temperature, and protein synthesis upon contact with epithelial cells. Infection and Immunity 64:966-973. PMID: 8641808.
57. Rotem E, Loinger A, Ronin I, Levin-Reisman I, Gabay C, Shoresh N, Biham O, Balaban NQ. 2010. Regulation of phenotypic variability by a threshold-based mechanism underlies bacterial persistence. PNAS 107:12541-12546.doi: 10.1073/pnas.1004333107, PMID: 20616060.
58. Schlosser-Silverman E, Elgrably-Weiss M, Rosenshine I, Kohen R, Altuvia S. 2000. Characterization of Escherichia coli DNA lesions generated within J774 macrophages. Journal of Bacteriology 182:5225-5230.doi: 10.1128/JB.182.18.5225-5230.2000, PMID: 10960109.
59. Silverman M, Simon M. 1980. Phase variation: genetic analysis of switching mutants. Cell 19:845-854.doi: 10.1016/0092-8674(80)90075-6, PMID: 6247071.
60. Smits WK, Kuipers OP, Veening JW. 2006. Phenotypic variation in bacteria: the role of feedback regulation. Nature Reviews Microbiology 4:259-271.doi: 10.1038/nrmicro1381, PMID: 16541134.
61. Somvanshi VS, Sloup RE, Crawford JM, Martin AR, Heidt AJ, Kim KS, Clardy J, Ciche TA. 2012. A single promoter inversion switches Photorhabdus between pathogenic and mutualistic states. Science 337:88-93.doi: 10.1126/science.1216641, PMID: 22767929.
62. Stewart MK, Cummings LA, Johnson ML, Berezow AB, Cookson BT. 2011. Regulation of phenotypic heterogeneity permits Salmonella evasion of the host caspase-1 inflammatory response. PNAS 108:20742-20747.doi: 10.1073/pnas.1108963108, PMID: 22143773.
63. Sturm A, Heinemann M, Arnoldini M, Benecke A, Ackermann M, Benz M, Dormann J, Hardt WD. 2011. The cost of virulence: retarded growth of Salmonella typhimurium cells expressing type III secretion system 1. PLoS Pathogens 7:e1002143.doi: 10.1371/journal.ppat.1002143, PMID: 21829349.
64. Süel GM, Garcia-Ojalvo J, Liberman LM, Elowitz MB. 2006. An excitable gene regulatory circuit induces transient cellular differentiation. Nature 440:545-550.doi: 10.1038/nature04588, PMID: 16554821.
65. Tan C, Marguet P, You L. 2009. Emergent bistability by a growth-modulating positive feedback circuit. Nature Chemical Biology 5:842-848.doi: 10.1038/nchembio.218, PMID: 19801994.
66. Temme K, Salis H, Tullman-Ercek D, Levskaya A, Hong SH, Voigt CA. 2008. Induction and relaxation dynamics of the regulatory network controlling the type III secretion system encoded within Salmonella pathogenicity island 1. Journal of Molecular Biology 377:47-61.doi: 10.1016/j.jmb.2007.12.044, PMID: 18242639.
67. Tobe T, Schoolnik GK, Sohel I, Bustamante VH, Puente JL. 1996. Cloning and characterization of bfpTVW, genes required for the transcriptional activation of bfpA in enteropathogenic Escherichia coli. Molecular Microbiology 21:963-975.doi: 10.1046/j.1365-2958.1996.531415.x, PMID: 8885267.
68. Tuchscherr L, Medina E, Hussain M, Völker W, Heitmann V, Niemann S, Holzinger D, Roth J, Proctor RA, Becker K, Peters G, Löffler B. 2011. Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Molecular Medicine 3:129-141.doi: 10.1002/emmm.201000115, PMID: 21268281.
69. Yerushalmi G, Nadler C, Berdichevski T, Rosenshine I. 2008. Mutational analysis of the locus of enterocyte effacement-encoded regulator (Ler) of enteropathogenic Escherichia coli. Journal of Bacteriology 190:7808-7818.doi: 10.1128/JB.00663-08, PMID: 18835988.