Abstract

Using oscillating optical tweezers, we show that controlled alignment of rod-shaped bacterial cells allows imaging fluorescently labeled three-dimensional (3D) subcellular structures from different, optimized viewpoints. To illustrate our method, we analyze the Z ring of E. coli. We obtain that the radial width of the Z ring in unconstricted cells is about 120 nm. This result suggests that the Z ring consists of an extremely sparse network of FtsZ filaments.

© 2012 Optical Society of America

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  1. R. H. Webb, Rep. Prog. Phys. 59, 427 (1996).
    [CrossRef]
  2. D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
    [CrossRef]
  3. J. B. Sibarita, Adv. Biochem. Eng. Biotechnol. 95, 201 (2005).
  4. K. Grunewald, O. Medalia, A. Gross, A. C. Steven, and W. Baumeister, Biophys. Chem. 100, 577 (2003).
    [CrossRef]
  5. G. Carmon and M. Feingold, Opt. Lett. 36, 40 (2011).
    [CrossRef]
  6. G. Carmon and M. Feingold, J. Nanophoton. 5, 051803 (2011).
    [CrossRef]
  7. D. W. Adams and J. Errington, Nat. Rev. Microbiol. 7, 642 (2009).
    [CrossRef]
  8. L. Zhuo, M. J. Trimble, Y. V. Brun, and G. J. Jensen, EMBO J. 26, 4694 (2007).
    [CrossRef]
  9. G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).
  10. J. Stricker, P. Maddox, E. D. Salmon, and H. P. Erickson, Proc. Natl. Acad. Sci. USA 99, 3171 (2002).
    [CrossRef]
  11. D. S. Weiss, J. Chen, J. Ghigo, D. Boyd, and J. Beckwith, J. Bacteriol. 181, 508 (1999).
  12. S. Thanedar and W. Margolin, Curr. Biol. 14, 1167 (2004).
    [CrossRef]
  13. R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
    [CrossRef]
  14. G. Reshes, S. Vanounou, I. Fishov, and M. Feingold, Biophys. J. 94, 251 (2008).
    [CrossRef]
  15. E. Itan, G. Carmon, A. Rabinovitch, I. Fishov, and M. Feingold, Phys. Rev. E 77, 061902 (2008).
    [CrossRef]
  16. M. Gu, Advanced Optical Imaging Theory (Springer-Verlag, 2000).

2011 (3)

G. Carmon and M. Feingold, Opt. Lett. 36, 40 (2011).
[CrossRef]

G. Carmon and M. Feingold, J. Nanophoton. 5, 051803 (2011).
[CrossRef]

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

2010 (1)

G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).

2009 (1)

D. W. Adams and J. Errington, Nat. Rev. Microbiol. 7, 642 (2009).
[CrossRef]

2008 (2)

G. Reshes, S. Vanounou, I. Fishov, and M. Feingold, Biophys. J. 94, 251 (2008).
[CrossRef]

E. Itan, G. Carmon, A. Rabinovitch, I. Fishov, and M. Feingold, Phys. Rev. E 77, 061902 (2008).
[CrossRef]

2007 (1)

L. Zhuo, M. J. Trimble, Y. V. Brun, and G. J. Jensen, EMBO J. 26, 4694 (2007).
[CrossRef]

2005 (1)

J. B. Sibarita, Adv. Biochem. Eng. Biotechnol. 95, 201 (2005).

2004 (1)

S. Thanedar and W. Margolin, Curr. Biol. 14, 1167 (2004).
[CrossRef]

2003 (1)

K. Grunewald, O. Medalia, A. Gross, A. C. Steven, and W. Baumeister, Biophys. Chem. 100, 577 (2003).
[CrossRef]

2002 (1)

J. Stricker, P. Maddox, E. D. Salmon, and H. P. Erickson, Proc. Natl. Acad. Sci. USA 99, 3171 (2002).
[CrossRef]

1999 (1)

D. S. Weiss, J. Chen, J. Ghigo, D. Boyd, and J. Beckwith, J. Bacteriol. 181, 508 (1999).

1996 (1)

R. H. Webb, Rep. Prog. Phys. 59, 427 (1996).
[CrossRef]

1991 (1)

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Adams, D. W.

D. W. Adams and J. Errington, Nat. Rev. Microbiol. 7, 642 (2009).
[CrossRef]

Baumeister, W.

K. Grunewald, O. Medalia, A. Gross, A. C. Steven, and W. Baumeister, Biophys. Chem. 100, 577 (2003).
[CrossRef]

Beckwith, J.

D. S. Weiss, J. Chen, J. Ghigo, D. Boyd, and J. Beckwith, J. Bacteriol. 181, 508 (1999).

Boyd, D.

D. S. Weiss, J. Chen, J. Ghigo, D. Boyd, and J. Beckwith, J. Bacteriol. 181, 508 (1999).

Brun, Y. V.

L. Zhuo, M. J. Trimble, Y. V. Brun, and G. J. Jensen, EMBO J. 26, 4694 (2007).
[CrossRef]

Buss, J.

G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).

Carmon, G.

G. Carmon and M. Feingold, J. Nanophoton. 5, 051803 (2011).
[CrossRef]

G. Carmon and M. Feingold, Opt. Lett. 36, 40 (2011).
[CrossRef]

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

E. Itan, G. Carmon, A. Rabinovitch, I. Fishov, and M. Feingold, Phys. Rev. E 77, 061902 (2008).
[CrossRef]

Chang, W.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Chen, J.

D. S. Weiss, J. Chen, J. Ghigo, D. Boyd, and J. Beckwith, J. Bacteriol. 181, 508 (1999).

Coltharp, C.

G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).

Erickson, H. P.

J. Stricker, P. Maddox, E. D. Salmon, and H. P. Erickson, Proc. Natl. Acad. Sci. USA 99, 3171 (2002).
[CrossRef]

Errington, J.

D. W. Adams and J. Errington, Nat. Rev. Microbiol. 7, 642 (2009).
[CrossRef]

Feingold, M.

G. Carmon and M. Feingold, J. Nanophoton. 5, 051803 (2011).
[CrossRef]

G. Carmon and M. Feingold, Opt. Lett. 36, 40 (2011).
[CrossRef]

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

G. Reshes, S. Vanounou, I. Fishov, and M. Feingold, Biophys. J. 94, 251 (2008).
[CrossRef]

E. Itan, G. Carmon, A. Rabinovitch, I. Fishov, and M. Feingold, Phys. Rev. E 77, 061902 (2008).
[CrossRef]

Fischer-Friedrich, E.

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

Fishov, I.

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

G. Reshes, S. Vanounou, I. Fishov, and M. Feingold, Biophys. J. 94, 251 (2008).
[CrossRef]

E. Itan, G. Carmon, A. Rabinovitch, I. Fishov, and M. Feingold, Phys. Rev. E 77, 061902 (2008).
[CrossRef]

Flotte, T.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Fu, G.

G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).

Fujimoto, J. G.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Ghigo, J.

D. S. Weiss, J. Chen, J. Ghigo, D. Boyd, and J. Beckwith, J. Bacteriol. 181, 508 (1999).

Gov, N. S.

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

Gregory, K.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Gross, A.

K. Grunewald, O. Medalia, A. Gross, A. C. Steven, and W. Baumeister, Biophys. Chem. 100, 577 (2003).
[CrossRef]

Grunewald, K.

K. Grunewald, O. Medalia, A. Gross, A. C. Steven, and W. Baumeister, Biophys. Chem. 100, 577 (2003).
[CrossRef]

Gu, M.

M. Gu, Advanced Optical Imaging Theory (Springer-Verlag, 2000).

Hee, M. R.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Hensel, Z.

G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).

Huang, D.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Huang, T.

G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).

Itan, E.

E. Itan, G. Carmon, A. Rabinovitch, I. Fishov, and M. Feingold, Phys. Rev. E 77, 061902 (2008).
[CrossRef]

Jensen, G. J.

L. Zhuo, M. J. Trimble, Y. V. Brun, and G. J. Jensen, EMBO J. 26, 4694 (2007).
[CrossRef]

Lin, C. P.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Maddox, P.

J. Stricker, P. Maddox, E. D. Salmon, and H. P. Erickson, Proc. Natl. Acad. Sci. USA 99, 3171 (2002).
[CrossRef]

Margolin, W.

S. Thanedar and W. Margolin, Curr. Biol. 14, 1167 (2004).
[CrossRef]

Medalia, O.

K. Grunewald, O. Medalia, A. Gross, A. C. Steven, and W. Baumeister, Biophys. Chem. 100, 577 (2003).
[CrossRef]

Puliafito, C. A.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Rabinovitch, A.

E. Itan, G. Carmon, A. Rabinovitch, I. Fishov, and M. Feingold, Phys. Rev. E 77, 061902 (2008).
[CrossRef]

Reshes, G.

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

G. Reshes, S. Vanounou, I. Fishov, and M. Feingold, Biophys. J. 94, 251 (2008).
[CrossRef]

Salmon, E. D.

J. Stricker, P. Maddox, E. D. Salmon, and H. P. Erickson, Proc. Natl. Acad. Sci. USA 99, 3171 (2002).
[CrossRef]

Schuman, J. S.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Sibarita, J. B.

J. B. Sibarita, Adv. Biochem. Eng. Biotechnol. 95, 201 (2005).

Steven, A. C.

K. Grunewald, O. Medalia, A. Gross, A. C. Steven, and W. Baumeister, Biophys. Chem. 100, 577 (2003).
[CrossRef]

Stinson, W. G.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Stricker, J.

J. Stricker, P. Maddox, E. D. Salmon, and H. P. Erickson, Proc. Natl. Acad. Sci. USA 99, 3171 (2002).
[CrossRef]

Swanson, E.

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Thanedar, S.

S. Thanedar and W. Margolin, Curr. Biol. 14, 1167 (2004).
[CrossRef]

Trimble, M. J.

L. Zhuo, M. J. Trimble, Y. V. Brun, and G. J. Jensen, EMBO J. 26, 4694 (2007).
[CrossRef]

Tsukanov, R.

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

Vanounou, S.

G. Reshes, S. Vanounou, I. Fishov, and M. Feingold, Biophys. J. 94, 251 (2008).
[CrossRef]

Webb, R. H.

R. H. Webb, Rep. Prog. Phys. 59, 427 (1996).
[CrossRef]

Weiss, D. S.

D. S. Weiss, J. Chen, J. Ghigo, D. Boyd, and J. Beckwith, J. Bacteriol. 181, 508 (1999).

Xiao, J.

G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).

Zhuo, L.

L. Zhuo, M. J. Trimble, Y. V. Brun, and G. J. Jensen, EMBO J. 26, 4694 (2007).
[CrossRef]

Adv. Biochem. Eng. Biotechnol. (1)

J. B. Sibarita, Adv. Biochem. Eng. Biotechnol. 95, 201 (2005).

Biophys. Chem. (1)

K. Grunewald, O. Medalia, A. Gross, A. C. Steven, and W. Baumeister, Biophys. Chem. 100, 577 (2003).
[CrossRef]

Biophys. J. (1)

G. Reshes, S. Vanounou, I. Fishov, and M. Feingold, Biophys. J. 94, 251 (2008).
[CrossRef]

Curr. Biol. (1)

S. Thanedar and W. Margolin, Curr. Biol. 14, 1167 (2004).
[CrossRef]

EMBO J. (1)

L. Zhuo, M. J. Trimble, Y. V. Brun, and G. J. Jensen, EMBO J. 26, 4694 (2007).
[CrossRef]

J. Bacteriol. (1)

D. S. Weiss, J. Chen, J. Ghigo, D. Boyd, and J. Beckwith, J. Bacteriol. 181, 508 (1999).

J. Nanophoton. (1)

G. Carmon and M. Feingold, J. Nanophoton. 5, 051803 (2011).
[CrossRef]

Nat. Rev. Microbiol. (1)

D. W. Adams and J. Errington, Nat. Rev. Microbiol. 7, 642 (2009).
[CrossRef]

Opt. Lett. (1)

Phys. Biol. (1)

R. Tsukanov, G. Reshes, G. Carmon, E. Fischer-Friedrich, N. S. Gov, I. Fishov, and M. Feingold, Phys. Biol. 8, 066003 (2011).
[CrossRef]

Phys. Rev. E (1)

E. Itan, G. Carmon, A. Rabinovitch, I. Fishov, and M. Feingold, Phys. Rev. E 77, 061902 (2008).
[CrossRef]

Plos ONE (1)

G. Fu, T. Huang, J. Buss, C. Coltharp, Z. Hensel, and J. Xiao, Plos ONE 5, e12680 (2010).

Proc. Natl. Acad. Sci. USA (1)

J. Stricker, P. Maddox, E. D. Salmon, and H. P. Erickson, Proc. Natl. Acad. Sci. USA 99, 3171 (2002).
[CrossRef]

Rep. Prog. Phys. (1)

R. H. Webb, Rep. Prog. Phys. 59, 427 (1996).
[CrossRef]

Science (1)

D. Huang, E. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, Science 254, 1178 (1991).
[CrossRef]

Other (1)

M. Gu, Advanced Optical Imaging Theory (Springer-Verlag, 2000).

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Figures (3)

Fig. 1.
Fig. 1.

The optical system: M1, M2, and M3–mirrors, L1, L2–telescope lenses, FC–filter cube. The laser beam is shown for the case when the galvanometric mirror is at 45° (solid red line) and for a smaller angle (dashed blue line).

Fig. 2.
Fig. 2.

A trapped unconstricted E. coli cell from a HIL experiment. All images are on the same scale. Bar=1μm. Left: horizontal orientation; Right: vertical orientation. (A) Phase contrast image, (B) FM4-64 image of the CM (red), (C) GFP image of the Z-ring (green), (D) overlay of (B) and (C). The weak red halo around the yellow ring indicates that the CM is farther from the cell axis than the Z ring.

Fig. 3.
Fig. 3.

Average radial profiles. (a) for the cell of Fig. 2: the profile of the CM (red circles) and the profile of the Z-ring (green triangles), rFM=411±3nm (right arrow), rGFP=356±5nm (left arrow), and Δr=54±6nm (rGFP denotes the position of the FtsZ-GFP I(r) peak). (b) Same as in (a) but for a model E. coli cell with a cylindrical surface Z ring (see text) (inset illustrates the corresponding midcell section). The radius of the model cell is set to 430 nm such that rFM is the same as in (a). Moreover, rZ-ring=389nm and Δr=21nm. (c) Same as in (b) but for a toroidal Z ring (see text). Here, rZ-ring=350nm and Δr=61nm.

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