1932

Abstract

Fluorescent proteins and developments in superresolution (nanoscopy) and single-molecule techniques bring high sensitivity, speed, and one order of magnitude gain in spatial resolution to live-cell imaging. These technologies have only recently been applied to prokaryotic cell biology, revealing the exquisite subcellular organization of bacterial cells. Here, we review the parallel evolution of fluorescence microscopy methods and their application to bacteria, mainly drawing examples from visualizing actin-like MreB proteins in the model bacterium . We describe the basic principles of nanoscopy and conventional techniques and their advantages and limitations to help microbiologists choose the most suitable technique for their biological question. Looking ahead, multidimensional live-cell nanoscopy combined with computational image analysis tools, systems biology approaches, and mathematical modeling will provide movie-like, mechanistic, and quantitative description of molecular events in bacterial cells.

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2014-09-08
2024-05-23
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Literature Cited

  1. Bashor CJ, Horwitz AA, Peisajovich SG, Lim WA. 1.  2010. Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems. Annu. Rev. Biophys. 39:515–37 [Google Scholar]
  2. Bendezu FO, Hale CA, Bernhardt TG, de Boer PA. 2.  2009. RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli.. EMBO J. 28:193–204 [Google Scholar]
  3. Berepiki A, Lichius A, Read ND. 3.  2011. Actin organization and dynamics in filamentous fungi. Nat. Rev. Microbiol. 9:876–87 [Google Scholar]
  4. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S. 4.  et al. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642–45 [Google Scholar]
  5. Bi EF, Lutkenhaus J. 5.  1991. FtsZ ring structure associated with division in Escherichia coli. Nature 354:161–64 [Google Scholar]
  6. Biggs DS. 6.  2010. 3D deconvolution microscopy. Curr. Protoc. Cytom. 12:12.19.1–20 [Google Scholar]
  7. Biteen JS, Moerner WE. 7.  2010. Single-molecule and superresolution imaging in live bacteria cells. Cold Spring Harb. Perspect. Biol. 2:a000448 [Google Scholar]
  8. Broder DH, Pogliano K. 8.  2006. Forespore engulfment mediated by a ratchet-like mechanism. Cell 126:917–28 [Google Scholar]
  9. Carballido-López R, Errington J. 9.  2003. The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev. Cell 4:19–28 [Google Scholar]
  10. Chastanet A, Carballido-López R. 10.  2012. The actin-like MreB proteins in Bacillus subtilis: a new turn. Front. Biosci. 4:1582–606 [Google Scholar]
  11. Christen B, Fero MJ, Hillson NJ, Bowman G, Hong S-H. 11.  et al. 2010. High-throughput identification of protein localization dependency networks. Proc. Natl. Acad. Sci. USA 107:4681–86 [Google Scholar]
  12. Dempsey GT, Vaughan JC, Chen KH, Bates M, Zhuang X. 12.  2011. Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat. Methods 8:1027–36 [Google Scholar]
  13. Dempwolff F, Moller HM, Graumann PL. 13.  2012. Synthetic motility and cell shape defects associated with deletions of flotillin/reggie paralogs in Bacillus subtilis and interplay of these proteins with NfeD proteins. J. Bacteriol. 194:4652–61 [Google Scholar]
  14. Dempwolff F, Wischhusen HM, Specht M, Graumann PL. 14.  2012. The deletion of bacterial dynamin and flotillin genes results in pleiotrophic effects on cell division, cell growth and in cell shape maintenance. BMC Microbiol. 12:298 [Google Scholar]
  15. Domínguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Söldner R, Carballido-López R. 15.  2011. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333:225–28 [Google Scholar]
  16. Elowitz MB, Surette MG, Wolf PE, Stock JB, Leibler S. 16.  1999. Protein mobility in the cytoplasm of Escherichia coli. J. Bacteriol. 181:197–203 [Google Scholar]
  17. English BP, Hauryliuk V, Sanamrad A, Tankov S, Dekker NH, Elf J. 17.  2011. Single-molecule investigations of the stringent response machinery in living bacterial cells. Proc. Natl. Acad. Sci. USA 108:E365–73 [Google Scholar]
  18. Fiche JB, Cattoni DI, Diekmann N, Langerak JM, Clerte C. 18.  et al. 2013. Recruitment, assembly, and molecular architecture of the SpoIIIE DNA pump revealed by superresolution microscopy. PLoS Biol. 11:e1001557 [Google Scholar]
  19. Fleming TC, Shin JY, Lee SH, Becker E, Huang KC. 19.  et al. 2010. Dynamic SpoIIIE assembly mediates septal membrane fission during Bacillus subtilis sporulation. Genes Dev. 24:1160–72 [Google Scholar]
  20. Fredlund J, Broder D, Fleming T, Claussin C, Pogliano K. 20.  2013. The SpoIIQ landmark protein has different requirements for septal localization and immobilization. Mol. Microbiol. 89:1053–68 [Google Scholar]
  21. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T. 21.  2011. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis.. Science 333:222–25 [Google Scholar]
  22. Goehring NW, Beckwith J. 22.  2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr. Biol. 15:R514–26 [Google Scholar]
  23. Goley ED, Dye NA, Werner JN, Gitai Z, Shapiro L. 23.  2010. Imaging-based identification of a critical regulator of FtsZ protofilament curvature in Caulobacter. Mol. Cell 39:975–87 [Google Scholar]
  24. Greenfield D, McEvoy AL, Shroff H, Crooks GE, Wingreen NS. 24.  et al. 2009. Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol. 7:e1000137 [Google Scholar]
  25. Gregory JA, Becker EC, Pogliano K. 25.  2008. Bacillus subtilis MinC destabilizes FtsZ-rings at new cell poles and contributes to the timing of cell division. Genes Dev. 22:3475–88 [Google Scholar]
  26. Guberman JM, Fay A, Dworkin J, Wingreen NS, Gitai Z. 26.  2008. PSICIC: noise and asymmetry in bacterial division revealed by computational image analysis at sub-pixel resolution. PLoS Comput. Biol. 4:e1000233 [Google Scholar]
  27. Gustafsson MG. 27.  2000. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 198:82–87 [Google Scholar]
  28. Ha T, Tinnefeld P. 28.  2012. Photophysics of fluorescent probes for single-molecule biophysics and super-resolution imaging. Annu. Rev. Phys. Chem. 63:595–617 [Google Scholar]
  29. Harke B, Ullal CK, Keller J, Hell SW. 29.  2008. Three-dimensional nanoscopy of colloidal crystals. Nano Lett. 8:1309–13 [Google Scholar]
  30. Hell SW. 30.  2007. Far-field optical nanoscopy. Science 316:1153–58 [Google Scholar]
  31. Hell SW, Wichmann J. 31.  1994. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19:780–82 [Google Scholar]
  32. Hess ST, Girirajan TP, Mason MD. 32.  2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91:4258–72 [Google Scholar]
  33. Huang B, Babcock H, Zhuang X. 33.  2010. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143:1047–58 [Google Scholar]
  34. Huang B, Jones SA, Brandenburg B, Zhuang X. 34.  2008. Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution. Nat. Methods 5:1047–52 [Google Scholar]
  35. Jackson D, Wang X, Rudner DZ. 35.  2012. Spatio-temporal organization of replication in bacteria and eukaryotes (nucleoids and nuclei). Cold Spring Harb. Perspect. Biol. 4:a010389 [Google Scholar]
  36. Jacobs C, Shapiro L. 36.  1999. Bacterial cell division: a moveable feast. Proc. Natl. Acad. Sci. USA 96:5891–93 [Google Scholar]
  37. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S. 37.  et al. 2008. Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5:695–702 [Google Scholar]
  38. Jones LJ, Carballido-López R, Errington J. 38.  2001. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913–22 [Google Scholar]
  39. Jones SA, Shim S-H, He J, Zhuang X. 39.  2011. Fast, three-dimensional super-resolution imaging of live cells. Nat. Methods 8:499–508 [Google Scholar]
  40. Jovanovic G, Mehta P, McDonald C, Davidson AC, Uzdavinys P. 40.  et al. 2013. The N-terminal amphipathic helices determine regulatory and effector functions of phage shock protein A (PspA) in Escherichia coli. J. Mol. Biol. 426:1498–1511 [Google Scholar]
  41. Juette MF, Gould TJ, Lessard MD, Mlodzianoski MJ, Nagpure BS. 41.  et al. 2008. Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples. Nat. Methods 5:527–29 [Google Scholar]
  42. Kentner D, Sourjik V. 42.  2010. Use of fluorescence microscopy to study intracellular signaling in bacteria. Annu. Rev. Microbiol. 64:373–90 [Google Scholar]
  43. Kim SY, Gitai Z, Kinkhabwala A, Shapiro L, Moerner WE. 43.  2006. Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 103:10929–34 [Google Scholar]
  44. Kirkpatrick CL, Viollier PH. 44.  2011. Poles apart: prokaryotic polar organelles and their spatial regulation. Cold Spring Harb. Perspect. Biol. 3:a006809 [Google Scholar]
  45. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E. 45.  et al. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12:291–99 [Google Scholar]
  46. Klar TA, Engel E, Hell SW. 46.  2001. Breaking Abbe's diffraction resolution limit in fluorescence microscopy with stimulated emission depletion beams of various shapes. Phys. Rev. E. 64:066613 [Google Scholar]
  47. Kner P, Chhun BB, Griffis ER, Winoto L, Gustafsson MGL. 47.  2009. Super-resolution video microscopy of live cells by structured illumination. Nat. Methods 6:339–42 [Google Scholar]
  48. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J. 48.  2012. Segregation of molecules at cell division reveals native protein localization. Nat. Methods 9:480–82 [Google Scholar]
  49. Leake MC, Chandler JH, Wadhams GH, Bai F, Berry RM, Armitage JP. 49.  2006. Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443:355–58 [Google Scholar]
  50. Lenn T, Leake MC, Mullineaux CW. 50.  2008. Clustering and dynamics of cytochrome bd-I complexes in the Escherichia coli plasma membrane in vivo. Mol. Microbiol. 70:1397–407 [Google Scholar]
  51. Li G, Brown PJ, Tang JX, Xu J, Quardokus EM. 51.  et al. 2012. Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol. Microbiol. 83:41–51 [Google Scholar]
  52. López D, Kolter R. 52.  2010. Functional microdomains in bacterial membranes. Genes Dev. 24:1893–902 [Google Scholar]
  53. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF. 53.  et al. 2008. High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat. Methods 5:155–57 [Google Scholar]
  54. Marston AL, Errington J. 54.  1999. Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol. Microbiol 33:84–96 [Google Scholar]
  55. Marston AL, Thomaides HB, Edwards DH, Sharpe ME, Errington J. 55.  1998. Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev. 12:3419–30 [Google Scholar]
  56. Meile J-C, Wu LJ, Ehrlich SD, Errington J, Noirot P. 56.  2006. Systematic localisation of proteins fused to the green fluorescent protein in Bacillus subtilis: identification of new proteins at the DNA replication factory. Proteomics 6:2135–46 [Google Scholar]
  57. Michie KA, Löwe J. 57.  2006. Dynamic filaments of the bacterial cytoskeleton. Annu. Rev. Biochem. 75:467–92 [Google Scholar]
  58. Mika JT, Poolman B. 58.  2011. Macromolecule diffusion and confinement in prokaryotic cells. Curr. Opin. Biotechnol. 22:117–26 [Google Scholar]
  59. Moseley JB, Goode BL. 59.  2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70:605–45 [Google Scholar]
  60. Mullineaux CW, Nenninger A, Ray N, Robinson C. 60.  2006. Diffusion of green fluorescent protein in three cell environments in Escherichia coli. J. Bacteriol. 188:3442–48 [Google Scholar]
  61. Murat D, Byrne M, Komeili A. 61.  2010. Cell biology of prokaryotic organelles. Cold Spring Harb. Perspect. Biol. 2:a000422 [Google Scholar]
  62. Niu L, Yu J. 62.  2008. Investigating intracellular dynamics of FtsZ cytoskeleton with photoactivation single-molecule tracking. Biophys. J. 95:2009–16 [Google Scholar]
  63. Olshausen PV, Defeu Soufo HJ, Wicker K, Heintzmann R, Graumann PL, Rohrbach A. 63.  2013. Superresolution imaging of dynamic MreB filaments in B. subtilis—a multiple-motor-driven transport?. Biophys. J. 105:1171–81 [Google Scholar]
  64. Patterson GH, Lippincott-Schwartz J. 64.  2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873–77 [Google Scholar]
  65. Persson F, Barkefors I, Elf J. 65.  2013. Single molecule methods with applications in living cells. Curr. Opin. Biotechnol. 24:737–44 [Google Scholar]
  66. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M. 66.  et al. 2010. A spindle-like apparatus guides bacterial chromosome segregation. Nat. Cell Biol. 12:791–98 [Google Scholar]
  67. Quirin S, Pavani SR, Piestun R. 67.  2012. Optimal 3D single-molecule localization for superresolution microscopy with aberrations and engineered point spread functions. Proc. Natl. Acad. Sci. USA 109:675–79 [Google Scholar]
  68. Rafelski SM, Marshall WF. 68.  2008. Building the cell: design principles of cellular architecture. Nat. Rev. Mol. Cell Biol. 9:593–602 [Google Scholar]
  69. Ramamurthi KS, Lecuyer S, Stone HA, Losick R. 69.  2009. Geometric cue for protein localization in a bacterium. Science 323:1354–57 [Google Scholar]
  70. Raskin DM, de Boer PA. 70.  1999. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. USA 96:4971–76 [Google Scholar]
  71. Reimold C, Defeu Soufo HJ, Dempwolff F, Graumann PL. 71.  2013. Motion of variable-length MreB filaments at the bacterial cell membrane influences cell morphology. Mol. Biol. Cell 24:2340–49 [Google Scholar]
  72. Rudner DZ, Losick R. 72.  2010. Protein subcellular localization in bacteria. Cold Spring Harb. Perspect. Biol. 2:a000307 [Google Scholar]
  73. Rueff AS, Chastanet A, Domínguez-Escobar J, Yao Z, Yates J. 73.  et al. 2013. An early cytoplasmic step of peptidoglycan synthesis is associated to MreB in Bacillus subtilis. Mol. Microbiol. 91:348–62 [Google Scholar]
  74. Rust MJ, Bates M, Zhuang X. 74.  2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3:793–95 [Google Scholar]
  75. Sako Y. 75.  2006. Imaging single molecules in living cells for systems biology. Mol. Syst. Biol. 2:56 [Google Scholar]
  76. Savage DF, Afonso B, Chen AH, Silver PA. 76.  2010. Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327:1258–61 [Google Scholar]
  77. Schlimpert S, Klein EA, Briegel A, Hughes V, Kahnt J. 77.  et al. 2012. General protein diffusion barriers create compartments within bacterial cells. Cell 151:1270–82 [Google Scholar]
  78. Sharp MD, Pogliano K. 78.  2002. Role of cell-specific SpoIIIE assembly in polarity of DNA transfer. Science 295:137–139 [Google Scholar]
  79. Shapiro L, McAdams HH, Losick R. 79.  2009. Why and how bacteria localize proteins. Science 326:1225–28 [Google Scholar]
  80. Sibarita JB. 80.  2005. Deconvolution microscopy. Adv. Biochem. Eng. Biotechnol. 95:201–43 [Google Scholar]
  81. Strauss MP, Liew AT, Turnbull L, Whitchurch CB, Monahan LG, Harry EJ. 81.  2012. 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol. 10:e1001389 [Google Scholar]
  82. Stricker J, Maddox P, Salmon ED, Erickson HP. 82.  2002. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl. Acad. Sci. USA 99:3171–75 [Google Scholar]
  83. Swulius MT, Jensen GJ. 83.  2012. The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-terminal yellow fluorescent protein tag. J. Bacteriol. 194:6382–86 [Google Scholar]
  84. Tokunaga M, Imamoto N, Sakata-Sogawa K. 84.  2008. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Methods 5:159–61 [Google Scholar]
  85. Tsien RY. 85.  1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509–44 [Google Scholar]
  86. Turner RD, Hurd AF, Cadby A, Hobbs JK, Foster SJ. 86.  2013. Cell wall elongation mode in gram-negative bacteria is determined by peptidoglycan architecture. Nat. Commun. 4:1496 [Google Scholar]
  87. Uphoff S, Reyes-Lamothe R, Garza de Leon F, Sherratt DJ, Kapanidis AN. 87.  2013. Single-molecule DNA repair in live bacteria. Proc. Natl. Acad. Sci. USA 110:8063–68 [Google Scholar]
  88. Wang W, Li G-W, Chen C, Xie XS, Zhuang X. 88.  2011. Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333:1445–49 [Google Scholar]
  89. Werner JN, Chen EY, Guberman JM, Zippilli AR, Irgon JJ, Gitai Z. 89.  2009. Quantitative genome-scale analysis of protein localization in an asymmetric bacterium. Proc. Natl. Acad. Sci. USA 106:7858–63 [Google Scholar]
  90. Xie XS, Choi PJ, Li G-W, Lee NK, Lia G. 90.  2008. Single-molecule approach to molecular biology in living bacterial cells. Annu. Rev. Biophys. 37:417–44 [Google Scholar]
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