The role of physiological heterogeneity in microbial population behavior (original) (raw)

References

  1. Maloney, P.C. & Rotman, B. Distribution of suboptimally induced β-D-galactosidase in Escherichia coli. The enzyme content of individual cells. J. Mol. Biol. 73, 77–91 (1973).
    Article CAS Google Scholar
  2. Siegele, D.A. & Hu, J.C. Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations. Proc. Natl. Acad. Sci. USA 94, 8168–8172 (1997).
    Article CAS Google Scholar
  3. Megerle, J.A., Fritz, G., Gerland, U., Jung, K. & Rädler, J.O. Timing and dynamics of single cell gene expression in the arabinose utilization system. Biophys. J. 95, 2103–2115 (2008).
    Article CAS Google Scholar
  4. Ghim, C.M. & Almaas, E. Genetic noise control via protein oligomerization. BMC Syst. Biol. 2, 94 (2008).
    Article Google Scholar
  5. Chastanet, A. et al. Broadly heterogeneous activation of the master regulator for sporulation in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 107, 8486–8491 (2010).
    Article CAS Google Scholar
  6. Chai, Y., Norman, T., Kolter, R. & Losick, R. An epigenetic switch governing daughter cell separation in Bacillus subtilis. Genes Dev. 24, 754–765 (2010).
    Article CAS Google Scholar
  7. López, D., Vlamakis, H., Losick, R. & Kolter, R. Cannibalism enhances biofilm development in Bacillus subtilis. Mol. Microbiol. 74, 609–618 (2009).
    Article Google Scholar
  8. Tan, C., Marguet, P. & You, L. Emergent bistability by a growth-modulating positive feedback circuit. Nat. Chem. Biol. 5, 842–848 (2009).
    Article CAS Google Scholar
  9. Kaern, M., Elston, T.C., Blake, W.J. & Collins, J.J. Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6, 451–464 (2005).
    Article CAS Google Scholar
  10. Booth, I.R. Stress and the single cell: intrapopulation diversity is a mechanism to ensure survival upon exposure to stress. Int. J. Food Microbiol. 78, 19–30 (2002).
    Article Google Scholar
  11. Thattai, M. & van Oudenaarden, A. Stochastic gene expression in fluctuating environments. Genetics 167, 523–530 (2004).
    Article Google Scholar
  12. Aertsen, A. & Michiels, C.W. Diversify or die: generation of diversity in response to stress. Crit. Rev. Microbiol. 31, 69–78 (2005).
    Article Google Scholar
  13. Locke, J.C. & Elowitz, M.B. Using movies to analyse gene circuit dynamics in single cells. Nat. Rev. Microbiol. 7, 383–392 (2009).
    Article CAS Google Scholar
  14. Longo, D. & Hasty, J. Dynamics of single-cell gene expression. Mol. Syst. Biol. 2, 64 (2006).
    Article Google Scholar
  15. Balaban, N.Q., Merrin, J., Chait, R., Kowalik, L. & Leibler, S. Bacterial persistence as a phenotypic switch. Science 305, 1622–1625 (2004).
    Article CAS Google Scholar
  16. Helaine, S. et al. Dynamics of intracellular bacterial replication at the single cell level. Proc. Natl. Acad. Sci. USA 107, 3746–3751 (2010).
    Article CAS Google Scholar
  17. Fraser, H.B., Hirsh, A.E., Giaever, G., Kumm, J. & Eisen, M.B. Noise minimization in eukaryotic gene expression. PLoS Biol. 2, e137 (2004).
    Article Google Scholar
  18. Rosenfeld, N., Young, J.W., Alon, U., Swain, P.S. & Elowitz, M.B. Gene regulation at the single-cell level. Science 307, 1962–1965 (2005).
    Article CAS Google Scholar
  19. Pedraza, J.M. & van Oudenaarden, A. Noise propagation in gene networks. Science 307, 1965–1969 (2005).
    Article CAS Google Scholar
  20. Colman-Lerner, A. et al. Regulated cell-to-cell variation in a cell-fate decision system. Nature 437, 699–706 (2005). Shows that growth rate variation in yeast is heritable and correlated with variation in gene expression.
    Article CAS Google Scholar
  21. Losick, R. & Desplan, C. Stochasticity and cell fate. Science 320, 65–68 (2008).
    Article CAS Google Scholar
  22. Zeng, Y., Novak, R., Shuga, J., Smith, M.T. & Mathies, R.A. High-performance single cell genetic analysis using microfluidic emulsion generator arrays. Anal. Chem. 82, 3183–3190 (2010).
    Article CAS Google Scholar
  23. Le, T.T. et al. Real-time RNA profiling within a single bacterium. Proc. Natl. Acad. Sci. USA 102, 9160–9164 (2005).
    Article CAS Google Scholar
  24. Golding, I., Paulsson, J., Zawilski, S.M. & Cox, E.C. Real-time kinetics of gene activity in individual bacteria. Cell 123, 1025–1036 (2005).
    Article CAS Google Scholar
  25. Becskei, A., Kaufmann, B.B. & van Oudenaarden, A. Contributions of low molecule number and chromosomal positioning to stochastic gene expression. Nat. Genet. 37, 937–944 (2005).
    Article CAS Google Scholar
  26. Kuang, Y., Biran, I. & Walt, D.R. Simultaneously monitoring gene expression kinetics and genetic noise in single cells by optical well arrays. Anal. Chem. 76, 6282–6286 (2004).
    Article CAS Google Scholar
  27. Newman, J.R. et al. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441, 840–846 (2006).
    Article CAS Google Scholar
  28. Anetzberger, C., Pirch, T. & Jung, K. Heterogeneity in quorum sensing-regulated bioluminescence of Vibrio harveyi. Mol. Microbiol. 73, 267–277 (2009).
    Article CAS Google Scholar
  29. Arriaga, E.A. Determining biological noise via single cell analysis. Anal. Bioanal. Chem. 393, 73–80 (2009).
    Article CAS Google Scholar
  30. Cai, L., Friedman, N. & Xie, X.S. Stochastic protein expression in individual cells at the single molecule level. Nature 440, 358–362 (2006).
    Article CAS Google Scholar
  31. Choi, P.J., Cai, L., Frieda, K. & Xie, X.S. A stochastic single-molecule event triggers phenotype switching of a bacterial cell. Science 322, 442–446 (2008).
    Article CAS Google Scholar
  32. Rajala, T., Häkkinen, A., Healy, S., Yli-Harja, O. & Ribeiro, A.S. Effects of transcriptional pausing on gene expression dynamics. PLoS Comput. Biol. 6, e1000704 (2010).
    Article Google Scholar
  33. Kussell, E., Kishony, R., Balaban, N.Q. & Leibler, S. Bacterial persistence: a model of survival in changing environments. Genetics 169, 1807–1814 (2005).
    Article Google Scholar
  34. Kussell, E. & Leibler, S. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309, 2075–2078 (2005). Proposes that phenotypic (physiological) diversity within populations would be a selective advantage in fluctuating environments, with bacterial persistence as an example.
    Article CAS Google Scholar
  35. Murphy, K.F., Balázsi, G. & Collins, J.J. Combinatorial promoter design for engineering noisy gene expression. Proc. Natl. Acad. Sci. USA 104, 12726–12731 (2007).
    Article CAS Google Scholar
  36. Freed, N.E. et al. A simple screen to identify promoters conferring high levels of phenotypic noise. PLoS Genet. 4, e1000307 (2008).
    Article Google Scholar
  37. Kelly, C.D. & Rahn, O. The growth rate of individual bacterial cells. J. Bacteriol. 23, 147–153 (1932).
    CAS PubMed PubMed Central Google Scholar
  38. Umehara, S., Wakamoto, Y., Inoue, I. & Yasuda, K. On-chip single-cell microcultivation assay for monitoring environmental effects on isolated cells. Biochem. Biophys. Res. Commun. 305, 534–540 (2003).
    Article CAS Google Scholar
  39. Pin, C. & Baranyi, J. Single-cell and population lag times as a function of cell age. Appl. Environ. Microbiol. 74, 2534–2536 (2008).
    Article CAS Google Scholar
  40. Strovas, T.J., Sauter, L.M., Guo, X. & Lidstrom, M.E. Cell-to-cell heterogeneity in growth rate and gene expression in Methylobacterium extorquens AM1. J. Bacteriol. 189, 7127–7133 (2007). Uses a flow-through system to follow individual cells through a shift in substrates, demonstrating that growth rate and gene expression are not correlated.
    Article CAS Google Scholar
  41. Strovas, T.J. & Lidstrom, M.E. Population heterogeneity in Methylobacterium extorquens AM1. Microbiology 155, 2040–2048 (2009).
    Article CAS Google Scholar
  42. Wang, P. et al. Robust growth of Escherichia coli. Curr. Biol. 20, 1099–1103 (2010).
    Article CAS Google Scholar
  43. Wegrzyn, A., Czyz, A., Gabig, M. & Wegrzyn, G. ClpP/ClpX-mediated degradation of the bacteriophage lambda O protein and regulation of lambda phage and lambda plasmid replication. Arch. Microbiol. 174, 89–96 (2000).
    Article CAS Google Scholar
  44. Ingham, C.J., Beerthuyzen, M. & van Hylckama Vlieg, J. Population heterogeneity of Lactobacillus plantarum WCFS1 microcolonies in response to and recovery from acid stress. Appl. Environ. Microbiol. 74, 7750–7758 (2008).
    Article CAS Google Scholar
  45. den Besten, H.M. et al. Quantitative analysis of population heterogeneity of the adaptive salt stress response and growth capacity of Bacillus cereus ATCC 14579. Appl. Environ. Microbiol. 73, 4797–4804 (2007).
    Article CAS Google Scholar
  46. Keren, I., Shah, D., Spoering, A., Kaldalu, N. & Lewis, K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol. 186, 8172–8180 (2004).
    Article CAS Google Scholar
  47. Liu, P. & Mathies, R.A. Integrated microfluidic systems for high-performance genetic analysis. Trends Biotechnol. 27, 572–581 (2009).
    Article CAS Google Scholar
  48. Muzzey, D. & van Oudenaarden, A. Quantitative time-lapse fluorescence microscopy in single cells. Annu. Rev. Cell Dev. Biol. 25, 301–327 (2009).
    Article CAS Google Scholar
  49. Wagner, M. Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu. Rev. Microbiol. 63, 411–429 (2009).
    Article CAS Google Scholar
  50. Amantonico, A., Urban, P.L. & Zenobi, R. Analytical techniques for single-cell metabolomics: state of the art and trends. Anal. Bioanal. Chem. published online, doi:10.1007/s00216–010–3850–1 (11 July 2010).
  51. Lindström, S. & Andersson-Svahn, H. Miniaturization of biological assays—overview on microwell devices for single-cell analyses. Biochim. Biophys. Acta published online, doi:10.1016/j.bbagen.2010.04.009 (6 May 2010).
  52. Zare, R.N. & Kim, S. Microfluidic platforms for single-cell analysis. Annu. Rev. Biomed. Eng. 12, 187–201 (2010).
    Article CAS Google Scholar
  53. Huang, W.E., Li, M., Jarvis, R.M., Goodacre, R. & Banwart, S.A. Shining light on the microbial world the application of Raman microspectroscopy. Adv. Appl. Microbiol. 70, 153–186 (2010).
    Article CAS Google Scholar
  54. Ishii, S., Tago, K. & Senoo, K. Single-cell analysis and isolation for microbiology and biotechnology: methods and applications. Appl. Microbiol. Biotechnol. 86, 1281–1292 (2010).
    Article CAS Google Scholar
  55. Shen, F., Du, W., Kreutz, J.E., Fok, A. & Ismagilov, R.F. Digital PCR on a SlipChip. Lab Chip published online, doi:10.1039/c004521g (1 July 2010).
  56. Shen, F. et al. Nanoliter multiplex PCR arrays on a SlipChip. Anal. Chem. 82, 4606–4612 (2010).
    Article CAS Google Scholar
  57. Vincent, M.E., Liu, W., Haney, E.B. & Ismagilov, R.F. Microfluidic stochastic confinement enhances analysis of rare cells by isolating cells and creating high density environments for control of diffusible signals. Chem. Soc. Rev. 39, 974–984 (2010).
    Article CAS Google Scholar
  58. Dragavon, J. et al. A cellular isolation system for real-time single-cell oxygen consumption monitoring. J. R. Soc. Interface 5 Suppl 2: S151–S159 (2008).
    CAS PubMed PubMed Central Google Scholar
  59. Sako, Y. Imaging single molecules in living cells for systems biology. Mol. Syst. Biol. 2, 56 (2006).
    Article Google Scholar
  60. Müller, D.J., Helenius, J., Alsteens, D. & Dufrene, Y.F. Force probing surfaces of living cells to molecular resolution. Nat. Chem. Biol. 5, 383–390 (2009).
    Article Google Scholar
  61. Yu, J., Xiao, J., Ren, X., Lao, K. & Xie, X.S. Probing gene expression in live cells, one protein molecule at a time. Science 311, 1600–1603 (2006).
    Article CAS Google Scholar
  62. Elf, J., Li, G.W. & Xie, X.S. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 316, 1191–1194 (2007).
    Article CAS Google Scholar
  63. Frunzke, J., Bramkamp, M., Schweitzer, J.E. & Bott, M. Population heterogeneity in Corynebacterium glutamicum ATCC 13032 caused by prophage CGP3. J. Bacteriol. 190, 5111–5119 (2008).
    Article CAS Google Scholar
  64. Niu, L. & Yu, J. Investigating intracellular dynamics of FtsZ cytoskeleton with photoactivation single-molecule tracking. Biophys. J. 95, 2009–2016 (2008).
    Article CAS Google Scholar
  65. Maamar, H., Raj, A. & Dubnau, D. Noise in gene expression determines cell fate in Bacillus subtilis. Science 317, 526 (2007).
    Article CAS Google Scholar
  66. Taniguchi, Y. et al. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329, 533–538 (2010).
    Article CAS Google Scholar
  67. Francius, G. et al. Detection, localization, and conformational analysis of single polysaccharide molecules on live bacteria. ACS Nano 2, 1921–1929 (2008).
    Article CAS Google Scholar
  68. Camesano, T.A. & Abu-Lail, N.I. Heterogeneity in bacterial surface polysaccharides, probed on a single-molecule basis. Biomacromolecules 3, 661–667 (2002).
    Article CAS Google Scholar
  69. Fritz, J., Katopodis, A.G., Kolbinger, F. & Anselmetti, D. Force-mediated kinetics of single P-selectin/ligand complexes observed by atomic force microscopy. Proc. Natl. Acad. Sci. USA 95, 12283–12288 (1998).
    Article CAS Google Scholar
  70. Shi, Q., Chien, Y.H. & Leckband, D. Biophysical properties of cadherin bonds do not predict cell sorting. J. Biol. Chem. 283, 28454–28463 (2008).
    Article CAS Google Scholar
  71. Kedrov, A., Janovjak, H., Sapra, K.T. & Muller, D.J. Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 36, 233–260 (2007).
    Article CAS Google Scholar
  72. Molter, T.W. et al. A microwell array device capable of measuring single-cell oxygen consumption rates. Sens. Actuators B Chem. 135, 678–686 (2009).
    Article CAS Google Scholar
  73. Kalyuzhnaya, M.G., Lidstrom, M.E. & Chistoserdova, L. Real-time detection of actively metabolizing microbes by redox sensing as applied to methylotroph populations in Lake Washington. ISME J. 2, 696–706 (2008).
    Article CAS Google Scholar
  74. Chao, T.C. & Ros, A. Microfluidic single-cell analysis of intracellular compounds. J. R. Soc. Interface 5 Suppl 2: S139–S150 (2008).
    CAS PubMed PubMed Central Google Scholar
  75. Kim, H.J., Boedicker, J.Q., Choi, J.W. & Ismagilov, R.F. Defined spatial structure stabilizes a synthetic multispecies bacterial community. Proc. Natl. Acad. Sci. USA 105, 18188–18193 (2008).
    Article CAS Google Scholar
  76. Liu, W., Kim, H.J., Lucchetta, E.M., Du, W. & Ismagilov, R.F. Isolation, incubation, and parallel functional testing and identification by FISH of rare microbial single-copy cells from multi-species mixtures using the combination of chemistrode and stochastic confinement. Lab Chip 9, 2153–2162 (2009). Uses water droplets generated in oil via microfluidics to isolate single cells, analyze them, allow growth and then split the cultures for downstream analyses.
    Article CAS Google Scholar
  77. Wang, D. & Bodovitz, S. Single cell analysis: the new frontier in 'omics'. Trends Biotechnol. 28, 281–290 (2010).
    Article CAS Google Scholar
  78. Masujima, T. Live single-cell mass spectrometry. Anal. Sci. 25, 953–960 (2009).
    Article CAS Google Scholar

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