Pre-Disposition and Epigenetics Govern Variation in Bacterial Survival upon Stress

English version České info

Bacteria suffer various stresses in their unpredictable environment. In response, clonal populations may exhibit cell-to-cell variation, hypothetically to maximize their survival. The origins, propagation, and consequences of this variability remain poorly understood. Variability persists through cell division events, yet detailed lineage information for individual stress-response phenotypes is scarce. This work combines time-lapse microscopy and microfluidics to uniformly manipulate the environmental changes experienced by clonal bacteria. We quantify the growth rates and RpoH-driven heat-shock responses of individual Escherichia coli within their lineage context, stressed by low streptomycin concentrations. We observe an increased variation in phenotypes, as different as survival from death, that can be traced to asymmetric division events occurring prior to stress induction. Epigenetic inheritance contributes to the propagation of the observed phenotypic variation, resulting in three-fold increase of the RpoH-driven expression autocorrelation time following stress induction. We propose that the increased permeability of streptomycin-stressed cells serves as a positive feedback loop underlying this epigenetic effect. Our results suggest that stochasticity, pre-disposition, and epigenetic effects are at the source of stress-induced variability. Unlike in a bet-hedging strategy, we observe that cells with a higher investment in maintenance, measured as the basal RpoH transcriptional activity prior to antibiotic treatment, are more likely to give rise to stressed, frail progeny.

Vyšlo v časopise: Pre-Disposition and Epigenetics Govern Variation in Bacterial Survival upon Stress. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003148
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003148

Souhrn

Zdroje

1. LidstromME, KonopkaMC (2010) The role of physiological heterogeneity in microbial population behavior. Nat Chem Biol 6 : 705–712.

2. EldarA, ElowitzMB (2010) Functional roles for noise in genetic circuits. Nature 467 : 167–173.

3. Bar-EvenA, PaulssonJ, MaheshriN, CarmiM, O'SheaE, et al. (2006) Noise in protein expression scales with natural protein abundance. Nat Genet 38 : 636–643.

4. TaniguchiY, ChoiPJ, LiGW, ChenHY, BabuM, et al. (2010) Quantifying E-coli Proteome and Transcriptome with Single-Molecule Sensitivity in Single Cells. Science 329 : 533–538.

5. NewmanJRS, GhaemmaghamiS, IhmelsJ, BreslowDK, NobleM, et al. (2006) Single-cell proteomic analysis of S-cerevisiae reveals the architecture of biological noise. Nature 441 : 840–846.

6. NovickA, WeinerM (1957) Enzyme Induction as an All-or-None Phenomenon. Proc Natl Acad Sci U S A 43 : 553–566.

7. VeeningJW, SmitsWK, KuipersOP (2008) Bistability, Epigenetics, and Bet-Hedging in Bacteria. Annu Rev Microbiol 62 : 193–210.

8. RobertL, PaulG, ChenY, TaddeiF, BaiglD, et al. (2010) Pre-dispositions and epigenetic inheritance in the Escherichia coli lactose operon bistable switch. Mol Syst Biol 6 : 357.

9. ZengLY, SkinnerSO, ZongCH, SippyJ, FeissM, et al. (2010) Decision Making at a Subcellular Level Determines the Outcome of Bacteriophage Infection. Cell 141 : 682–691.

10. VeeningJW, StewartEJ, BerngruberTW, TaddeiF, KuipersOP, et al. (2008) Bet-hedging and epigenetic inheritance in bacterial cell development. Proc Natl Acad Sci U S A 105 : 4393–4398.

11. SnijderB, PelkmansL (2011) Origins of regulated cell-to-cell variability. Nat Rev Mol Cell Biol 12 : 119–125.

12. BlakeWJ, BalazsiG, KohanskiMA, IsaacsFJ, MurphyKF, et al. (2006) Phenotypic consequences of promoter-mediated transcriptional noise. Mol Cell 24 : 853–865.

13. FraserD, KaernM (2009) A chance at survival: gene expression noise and phenotypic diversification strategies. Mol Microbiol 71 : 1333–1340.

14. BalabanNQ, MerrinJ, ChaitR, KowalikL, LeiblerS (2004) Bacterial persistence as a phenotypic switch. Science 305 : 1622–1625.

15. KussellE, LeiblerS (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309 : 2075–2078.

16. D'CostaVM, KingCE, KalanL, MorarM, SungWWL, et al. (2011) Antibiotic resistance is ancient. Nature 477 : 457–461.

17. MagnetS, BlanchardJS (2005) Molecular insights into aminoglycoside action and resistance. Chem Rev 105 : 477–497.

18. KohanskiMA, DwyerDJ, WierzbowskiJ, CottarelG, CollinsJJ (2008) Mistranslation of Membrane Proteins and Two-Component System Activation Trigger Antibiotic-Mediated Cell Death. Cell 135 : 679–690.

19. FontaineF, StewartEJ, LindnerAB, TaddeiF (2008) Mutations in two global regulators lower individual mortality in Escherichia coli. Mol Microbiol 67 : 2–14.

20. KraftM, KnupferU, WenderothR, PietschmannP, HockB, et al. (2007) An online monitoring system based on a synthetic sigma32-dependent tandem promoter for visualization of insoluble proteins in the cytoplasm of Escherichia coli. Appl Microbiol Biotechnol 75 : 397–406.

21. Primet M, Demarez A, Taddei F, Lindner AB, Moisan L (2008) Tracking of cells in a sequence of images using a low-dimension image representation. 2008 Ieee International Symposium on Biomedical Imaging: from Nano to Macro, Vols 1–4. New York: Ieee. pp. 995–998.

22. SigalA, MiloR, CohenA, Geva-ZatorskyN, KleinY, et al. (2006) Variability and memory of protein levels in human cells. Nature 444 : 643–646.

23. DavisBD, ChenLL, TaiPC (1986) Misread Protein Creates Membrane Channels -⁠ an Essential Step in the Bactericidal Action of Aminoglycosides. Proc Natl Acad Sci U S A 83 : 6164–6168.

24. AnandN, DavisBD (1960) Effect of Streptomycin on Escherichia-Coli. Nature 185 : 22–23.

25. DelcourAH (2009) Outer membrane permeability and antibiotic resistance. Biochim Biophys Acta -Proteins and Proteomics 1794 : 808–816.

26. TaberHW, MuellerJP, MillerPF, ArrowAS (1987) Bacterial Uptake of Aminoglycoside Antibiotics. Microbiol Rev 51 : 439–457.

27. SiglerA, SchubertP, HillenW, NiederweisM (2000) Permeation of tetracyclines through membranes of liposomes and Escherichia coli. Eur J Biochem 267 : 527–534.

28. HuhD, PaulssonJ (2011) Non-genetic heterogeneity from stochastic partitioning at cell division. Nat Genet 43 : 95–100.

29. NinioJ (1991) Connections between Translation, Transcription and Replication Error-Rates. Biochimie 73 : 1517–1523.

30. LindnerAB, DemarezA (2009) Protein aggregation as a paradigm of aging. Biochim Biophys Acta -General Subjects 1790 : 980–996.

31. DaviesJ, SpiegelmanGB, YimG (2006) The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 9 : 445–453.

32. KohanskiMA, DwyerDJ, HayeteB, LawrenceCA, CollinsJJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130 : 797–810.

33. NicholsRJ, SenS, ChooYJ, BeltraoP, ZietekM, et al. (2011) Phenotypic Landscape of a Bacterial Cell. Cell 144 : 143–156.

34. ZhangQC, LambertG, LiaoD, KimH, RobinK, et al. (2011) Acceleration of Emergence of Bacterial Antibiotic Resistance in Connected Microenvironments. Science 333 : 1764–1767.

35. LeiblerS, KussellE (2010) Individual histories and selection in heterogeneous populations. Proc Natl Acad Sci U S A 107 : 13183–13188.

36. BlattnerFR, PlunkettG, BlochCA, PernaNT, BurlandV, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277 : 1453–1462.

37. GiraudA, ArousS, De PaepeM, Gaboriau-RouthiauV, BambouJC, et al. (2008) Dissecting the genetic components of adaptation of Escherichia coli to the mouse gut. PLoS Genet 4: e2 doi:10.1371/journal.pgen.0040002.

38. LindnerAB, MaddenR, DernarezA, StewartEJ, TaddeiF (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci U S A 105 : 3076–3081.

39. StewartEJ, MaddenR, PaulG, TaddeiF (2005) Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol 3: e45 doi:10.1371/journal.pbio.0030045.