Fluorescence imaging for bacterial cell biology: From localization to dynamics, from ensembles to single molecules

Annual Review of Microbiology

Volumn 68, Issue , 2014, Pages 459-476

  Yao, Zhizhong ^a   Carballido López, Rut ^a  

^a UMR1319 MICALIS   (France)

Author keywords

Bacterial cytoskeleton; MreB; Protein subcellular localization; Single molecule; Superresolution

Indexed keywords

FLUORESCENT DYE; BACTERIAL PROTEIN;

BACILLUS SUBTILIS; BACTERIAL CELL; CELLULAR DISTRIBUTION; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; NONHUMAN; PROTEIN LOCALIZATION; REVIEW; CHEMISTRY; EVALUATION STUDY; GENETICS; METABOLISM; NANOTECHNOLOGY; PROCEDURES;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; MICROSCOPY, FLUORESCENCE; NANOTECHNOLOGY;

EID: 84907479598     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-091213-113034     Document Type: Review

References (90)

1. Bashor CJ, Horwitz AA, Peisajovich SG, Lim WA. 2010. Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems. Annu. Rev. Biophys. 39:515-37
2. Bendezu FO, Hale CA, Bernhardt TG, de Boer PA. 2009. RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli. EMBO J. 28:193-204
3. Berepiki A, Lichius A, Read ND. 2011. Actin organization and dynamics in filamentous fungi. Nat. Rev. Microbiol. 9:876-87
4. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, et al. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642-45
5. Bi EF, Lutkenhaus J. 1991. FtsZ ring structure associated with division in Escherichia coli. Nature 354:161-64
6. Biggs DS. 2010. 3D deconvolution microscopy. Curr. Protoc. Cytom. 12:12.19.1-20
7. Biteen JS, Moerner WE. 2010. Single-molecule and superresolution imaging in live bacteria cells. Cold Spring Harb. Perspect. Biol. 2:a000448
8. BroderDH, PoglianoK. 2006. Forespore engulfmentmediated by a ratchet-likemechanism. Cell 126:917-28
9. Carballido-Lopez R, Errington J. 2003. The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev. Cell 4:19-28
10. Chastanet A,Carballido-Lopez R. 2012. The actin-likeMreB proteins in Bacillus subtilis: a new turn. Front. Biosci. 4:1582-606
11. Christen B, Fero MJ, Hillson NJ, Bowman G, Hong S-H, et al. 2010. High-throughput identification of protein localization dependency networks. Proc. Natl. Acad. Sci. USA 107:4681-86
12. Dempsey GT, Vaughan JC, Chen KH, Bates M, Zhuang X. 2011. Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat. Methods 8:1027-36
13. Dempwolff F,Moller HM, Graumann PL. 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
14. Dempwolff F,Wischhusen HM, Specht M, Graumann PL. 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
15. Dominguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Soldner R, Carballido-Lopez R. 2011. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333:225-28
16. Elowitz MB, Surette MG, Wolf PE, Stock JB, Leibler S. 1999. Protein mobility in the cytoplasm of Escherichia coli. J. Bacteriol. 181:197-203
17. English BP, HauryliukV, Sanamrad A,Tankov S,DekkerNH, Elf J. 2011. Single-molecule investigations of the stringent response machinery in living bacterial cells. Proc. Natl. Acad. Sci. USA 108:E365-73
18. Fiche JB, Cattoni DI, Diekmann N, Langerak JM, Clerte C, et al. 2013. Recruitment, assembly, and molecular architecture of the SpoIIIE DNA pump revealed by superresolution microscopy. PLoS Biol. 11:e1001557
19. Fleming TC, Shin JY, Lee SH, Becker E, Huang KC, et al. 2010. Dynamic SpoIIIE assembly mediates septal membrane fission during Bacillus subtilis sporulation. Genes Dev. 24:1160-72
20. Fredlund J, Broder D, Fleming T, Claussin C, Pogliano K. 2013. The SpoIIQ landmark protein has different requirements for septal localization and immobilization. Mol. Microbiol. 89:1053-68
21. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T. 2011. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333:222-25
22. Goehring NW, Beckwith J. 2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr. Biol. 15:R514-26
23. Goley ED, Dye NA, Werner JN, Gitai Z, Shapiro L. 2010. Imaging-based identification of a critical regulator of FtsZ protofilament curvature in Caulobacter. Mol. Cell 39:975-87
24. Greenfield D, McEvoy AL, Shroff H, Crooks GE, Wingreen NS, et al. 2009. Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol. 7:e1000137
25. Gregory JA, Becker EC, Pogliano K. 2008. Bacillus subtilis MinC destabilizes FtsZ-rings at new cell poles and contributes to the timing of cell division. Genes Dev. 22:3475-88
26. Guberman JM, Fay A, Dworkin J,Wingreen NS,Gitai Z. 2008. PSICIC: noise and asymmetry in bacterial division revealed by computational image analysis at sub-pixel resolution. PLoS Comput. Biol. 4:e1000233
27. Gustafsson MG. 2000. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 198:82-87
28. Ha T, Tinnefeld P. 2012. Photophysics of fluorescent probes for single-molecule biophysics and superresolution imaging. Annu. Rev. Phys. Chem. 63:595-617
29. Harke B, Ullal CK, Keller J, Hell SW. 2008. Three-dimensional nanoscopy of colloidal crystals. Nano Lett. 8:1309-13
30. Hell SW. 2007. Far-field optical nanoscopy. Science 316:1153-58
31. Hell SW,Wichmann J. 1994. Breaking the diffraction resolution limit by stimulated emission: stimulatedemission- depletion fluorescence microscopy. Opt. Lett. 19:780-82
32. Hess ST,Girirajan TP, MasonMD. 2006. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91:4258-72
33. Huang B, Babcock H, Zhuang X. 2010. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143:1047-58
34. Huang B, Jones SA, Brandenburg B, Zhuang X. 2008. Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution. Nat. Methods 5:1047-52
35. Jackson D, Wang X, Rudner DZ. 2012. Spatio-temporal organization of replication in bacteria and eukaryotes (nucleoids and nuclei). Cold Spring Harb. Perspect. Biol. 4:a010389
36. Jacobs C, Shapiro L. 1999. Bacterial cell division: a moveable feast. Proc. Natl. Acad. Sci. USA 96:5891-93
37. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S, et al. 2008. Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5:695-702
38. Jones LJ, Carballido-Lopez R, Errington J. 2001. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913-22
39. Jones SA, Shim S-H, He J, Zhuang X. 2011. Fast, three-dimensional super-resolution imaging of live cells. Nat. Methods 8:499-508
40. JovanovicG,Mehta P, McDonald C, Davidson AC,Uzdavinys P, et al. 2013. TheN-terminal amphipathic helices determine regulatory and effector functions of phage shock protein A (PspA) in Escherichia coli. J. Mol. Biol. 426:1498-1511
41. Juette MF, Gould TJ, Lessard MD, Mlodzianoski MJ, Nagpure BS, et al. 2008. Three-dimensional sub- 100 nm resolution fluorescence microscopy of thick samples. Nat. Methods 5:527-29
42. Kentner D, Sourjik V. 2010. Use of fluorescence microscopy to study intracellular signaling in bacteria. Annu. Rev. Microbiol. 64:373-90
43. Kim SY, Gitai Z, Kinkhabwala A, Shapiro L, Moerner WE. 2006. Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 103:10929-34
44. Kirkpatrick CL, Viollier PH. 2011. Poles apart: prokaryotic polar organelles and their spatial regulation. Cold Spring Harb. Perspect. Biol. 3:a006809
45. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, 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
46. Klar TA, Engel E, Hell SW. 2001. Breaking Abbes diffraction resolution limit in fluorescencemicroscopy with stimulated emission depletion beams of various shapes. Phys. Rev. E. 64:066613
47. Kner P, Chhun BB, Griffis ER, Winoto L, Gustafsson MGL. 2009. Super-resolution video microscopy of live cells by structured illumination. Nat. Methods 6:339-42
48. Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J. 2012. Segregation of molecules at cell division reveals native protein localization. Nat. Methods 9:480-82
49. Leake MC, Chandler JH, Wadhams GH, Bai F, Berry RM, Armitage JP. 2006. Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443:355-58
50. Lenn T, Leake MC, Mullineaux CW. 2008. Clustering and dynamics of cytochrome bd-I complexes in the Escherichia coli plasma membrane in vivo. Mol. Microbiol. 70:1397-407
51. Li G, Brown PJ, Tang JX, Xu J, Quardokus EM, et al. 2012. Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol. Microbiol. 83:41-51
52. L opez D, Kolter R. 2010. Functional microdomains in bacterial membranes. Genes Dev. 24:1893-902
53. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, et al. 2008. High-density mapping of singlemolecule trajectories with photoactivated localization microscopy. Nat. Methods 5:155-57
54. Marston AL, Errington J.1999. Selection of the midcell division site in Bacillus subtilis through MinDdependent polar localization and activation of MinC. Mol. Microbiol. 33:84-96
55. Marston AL, Thomaides HB, Edwards DH, SharpeME, Errington J. 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
56. Meile J-C, Wu LJ, Ehrlich SD, Errington J, Noirot P. 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
57. Michie KA, Löwe J. 2006. Dynamic filaments of the bacterial cytoskeleton. Annu. Rev. Biochem. 75:467-92
58. Mika JT, Poolman B. 2011. Macromolecule diffusion and confinement in prokaryotic cells. Curr. Opin. Biotechnol. 22:117-26
59. Moseley JB, Goode BL. 2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70:605-45
60. Mullineaux CW, Nenninger A, Ray N, Robinson C. 2006. Diffusion of green fluorescent protein in three cell environments in Escherichia coli. J. Bacteriol. 188:3442-48
61. Murat D, Byrne M, Komeili A. 2010. Cell biology of prokaryotic organelles. Cold Spring Harb. Perspect. Biol. 2:a000422
62. Niu L, Yu J. 2008. Investigating intracellular dynamics of FtsZ cytoskeleton with photoactivation singlemolecule tracking. Biophys. J. 95:2009-16
63. Olshausen PV, Defeu Soufo HJ, Wicker K, Heintzmann R, Graumann PL, Rohrbach A. 2013. Superresolution imaging of dynamic MreB filaments in B. subtilis-a multiple-motor-driven transport? Biophys. J. 105:1171-81
64. Patterson GH, Lippincott-Schwartz J. 2002. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873-77
65. Persson F, Barkefors I, Elf J. 2013. Single molecule methods with applications in living cells. Curr. Opin. Biotechnol. 24:737-44
66. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M, et al. 2010. A spindle-like apparatus guides bacterial chromosome segregation. Nat. Cell Biol. 12:791-98
67. Quirin S, Pavani SR, Piestun R. 2012. Optimal 3D single-molecule localization for superresolution microscopy with aberrations and engineered point spread functions. Proc. Natl. Acad. Sci. USA 109:675-79
68. Rafelski SM, Marshall WF. 2008. Building the cell: design principles of cellular architecture. Nat. Rev. Mol. Cell Biol. 9:593-602
69. Ramamurthi KS, Lecuyer S, Stone HA, Losick R. 2009. Geometric cue for protein localization in a bacterium. Science 323:1354-57
70. Raskin DM, de Boer PA. 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
71. Reimold C, Defeu Soufo HJ, Dempwolff F, Graumann PL. 2013. Motion of variable-length MreB filaments at the bacterial cell membrane influences cell morphology. Mol. Biol. Cell 24:2340-49
72. Rudner DZ, Losick R. 2010. Protein subcellular localization in bacteria. Cold Spring Harb. Perspect. Biol. 2:a000307
73. Rueff AS, Chastanet A, Dominguez-Escobar J, Yao Z, Yates J, et al. 2013. An early cytoplasmic step of peptidoglycan synthesis is associated to MreB in Bacillus subtilis. Mol. Microbiol. 91:348-62
74. Rust MJ, Bates M, Zhuang X. 2006. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3:793-95
75. Sako Y. 2006. Imaging single molecules in living cells for systems biology. Mol. Syst. Biol. 2:56
76. Savage DF, Afonso B, Chen AH, Silver PA. 2010. Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327:1258-61
77. Schlimpert S, Klein EA, Briegel A, Hughes V, Kahnt J, et al. 2012. General protein diffusion barriers create compartments within bacterial cells. Cell 151:1270-82
78. Sharp MD, Pogliano K. 2002. Role of cell-specific SpoIIIE assembly in polarity of DNA transfer. Science 295:137-139
79. Shapiro L, McAdams HH, Losick R. 2009. Why and how bacteria localize proteins. Science 326:1225-28
80. Sibarita JB. 2005. Deconvolution microscopy. Adv. Biochem. Eng. Biotechnol. 95:201-43
81. Strauss MP, Liew AT, Turnbull L, Whitchurch CB, Monahan LG, Harry EJ. 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
82. Stricker J, Maddox P, Salmon ED, Erickson HP. 2002. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc.Natl. Acad. Sci.USA99:3171-75
83. Swulius MT, Jensen GJ. 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
84. Tokunaga M, Imamoto N, Sakata-Sogawa K. 2008. Highly inclined thin illumination enables clear singlemolecule imaging in cells. Nat. Methods 5:159-61
85. Tsien RY. 1998. The green fluorescent protein. Annu. Rev. Biochem. 67:509-44
86. Turner RD, Hurd AF, Cadby A, Hobbs JK, Foster SJ. 2013. Cell wall elongation mode in gram-negative bacteria is determined by peptidoglycan architecture. Nat. Commun. 4:1496
87. Uphoff S, Reyes-Lamothe R, Garza de Leon F, Sherratt DJ, Kapanidis AN. 2013. Single-molecule DNA repair in live bacteria. Proc. Natl. Acad. Sci. USA 110:8063-68
88. Wang W, Li G-W, Chen C, Xie XS, Zhuang X. 2011. Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333:1445-49
89. Werner JN, Chen EY, Guberman JM, Zippilli AR, Irgon JJ, Gitai Z. 2009. Quantitative genome-scale analysis of protein localization in an asymmetric bacterium. Proc. Natl. Acad. Sci. USA 106:7858-63
90. Xie XS, Choi PJ, LiG-W, Lee NK, Lia G. 2008. Single-molecule approach to molecular biology in living bacterial cells. Annu. Rev. Biophys. 37:417-44