Abstract

Elucidating chromatin structure in vitro requires resolution below 10 nm to visualize the mononucleosome has been an ongoing challenge. In this work, we achieve sub-10-nm imaging of nucleic acids via spectroscopic intrinsic-contrast photon-localization optical nanoscopy (SICLON) without the use of external labels. SICLON leverages two key innovations: using endogenous nucleotides as the emission source and a custom-made imaging system that can simultaneously record the position and optical spectra of emitting molecules. With a novel spectral regression algorithm that identifies the spectroscopic fingerprints of neighboring molecules that were previously indistinguishable, we demonstrate the utility of SICLON by visualizing unlabeled poly-nucleotides and linear single-stranded DNA fibers with a resolution of 6.2 nm.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2017 (3)

H. D. Ou, S. Phan, T. J. Deerinck, A. Thor, M. H. Ellisman, and C. C. O’Shea, Science 357, eaag0025 (2017).
[Crossref]

B. Dong, L. M. Almassalha, B. T. Soetikno, J. E. Chandler, B. E. Urban, C. Sun, H. F. Zhang, and V. Backman, Opt. Express 25, 7929 (2017).
[Crossref]

J. Schnitzbauer, M. T. Strauss, T. Schlichthaerle, F. Schueder, and R. Jungmann, Nat. Protoc. 12, 1198 (2017).
[Crossref]

2016 (3)

B. Dong, L. M. Almassalha, Y. Stypula-Cyrus, B. E. Urban, J. E. Chandler, C. Sun, H. F. Zhang, and V. Backman, Proc. Natl. Acad. Sci. USA 113, 9716 (2016).
[Crossref]

S. Wang, J.-H. Su, B. J. Beliveau, B. Bintu, J. R. Moffitt, C.-T. Wu, and X. Zhuang, Science 353, 598 (2016).
[Crossref]

B. Dong, L. Almassalha, B. E. Urban, S. Khuon, T.-L. Chew, V. Backman, C. Sun, and H. F. Zhang, Nat. Commun. 7, 12290 (2016).
[Crossref]

2014 (1)

M. Ovesný, P. Křížek, J. Borkovec, Z. Švindrych, and G. M. Hagen, Bioinformatics 30, 2389 (2014).
[Crossref]

2012 (2)

K. Xu, H. P. Babcock, and X. Zhuang, Nat. Methods 9, 185 (2012).
[Crossref]

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

2011 (2)

R. Henriques, C. Griffiths, E. Hesper Rego, and M. M. Mhlanga, Biopolymers 95, 322 (2011).
[Crossref]

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

2003 (1)

R. J. Ellis and A. P. Minton, Nature 425, 27 (2003).
[Crossref]

2000 (1)

J. M. Harp, B. L. Hanson, D. E. Timm, and G. J. Bunick, Acta Crystallogr. Sect. D 56, 1513 (2000).
[Crossref]

1999 (1)

H. Yokota, J. Sunwoo, M. Sarikaya, G. van den Engh, and R. Aebersold, Anal. Chem. 71, 4418 (1999).
[Crossref]

1997 (1)

K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent, and T. J. Richmond, Nature 389, 251 (1997).
[Crossref]

Aebersold, R.

H. Yokota, J. Sunwoo, M. Sarikaya, G. van den Engh, and R. Aebersold, Anal. Chem. 71, 4418 (1999).
[Crossref]

Almassalha, L.

B. Dong, L. Almassalha, B. E. Urban, S. Khuon, T.-L. Chew, V. Backman, C. Sun, and H. F. Zhang, Nat. Commun. 7, 12290 (2016).
[Crossref]

Almassalha, L. M.

B. Dong, L. M. Almassalha, B. T. Soetikno, J. E. Chandler, B. E. Urban, C. Sun, H. F. Zhang, and V. Backman, Opt. Express 25, 7929 (2017).
[Crossref]

B. Dong, L. M. Almassalha, Y. Stypula-Cyrus, B. E. Urban, J. E. Chandler, C. Sun, H. F. Zhang, and V. Backman, Proc. Natl. Acad. Sci. USA 113, 9716 (2016).
[Crossref]

Apostolopoulos, N.

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Babcock, H. P.

K. Xu, H. P. Babcock, and X. Zhuang, Nat. Methods 9, 185 (2012).
[Crossref]

Backman, V.

B. Dong, L. M. Almassalha, B. T. Soetikno, J. E. Chandler, B. E. Urban, C. Sun, H. F. Zhang, and V. Backman, Opt. Express 25, 7929 (2017).
[Crossref]

B. Dong, L. M. Almassalha, Y. Stypula-Cyrus, B. E. Urban, J. E. Chandler, C. Sun, H. F. Zhang, and V. Backman, Proc. Natl. Acad. Sci. USA 113, 9716 (2016).
[Crossref]

B. Dong, L. Almassalha, B. E. Urban, S. Khuon, T.-L. Chew, V. Backman, C. Sun, and H. F. Zhang, Nat. Commun. 7, 12290 (2016).
[Crossref]

Beliveau, B. J.

S. Wang, J.-H. Su, B. J. Beliveau, B. Bintu, J. R. Moffitt, C.-T. Wu, and X. Zhuang, Science 353, 598 (2016).
[Crossref]

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Benke, A.

P. J. Fabre, A. Benke, S. Manley, and D. Duboule, Cold Spring Harbor Symposia on Quantitative Biology (Cold Spring Harbor Laboratory, 2015), pp. 9–16.

Bintu, B.

S. Wang, J.-H. Su, B. J. Beliveau, B. Bintu, J. R. Moffitt, C.-T. Wu, and X. Zhuang, Science 353, 598 (2016).
[Crossref]

Borkovec, J.

M. Ovesný, P. Křížek, J. Borkovec, Z. Švindrych, and G. M. Hagen, Bioinformatics 30, 2389 (2014).
[Crossref]

Bunick, G. J.

J. M. Harp, B. L. Hanson, D. E. Timm, and G. J. Bunick, Acta Crystallogr. Sect. D 56, 1513 (2000).
[Crossref]

Causse, S.

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

Chandler, J. E.

B. Dong, L. M. Almassalha, B. T. Soetikno, J. E. Chandler, B. E. Urban, C. Sun, H. F. Zhang, and V. Backman, Opt. Express 25, 7929 (2017).
[Crossref]

B. Dong, L. M. Almassalha, Y. Stypula-Cyrus, B. E. Urban, J. E. Chandler, C. Sun, H. F. Zhang, and V. Backman, Proc. Natl. Acad. Sci. USA 113, 9716 (2016).
[Crossref]

Chang, Y.

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Chew, T.-L.

B. Dong, L. Almassalha, B. E. Urban, S. Khuon, T.-L. Chew, V. Backman, C. Sun, and H. F. Zhang, Nat. Commun. 7, 12290 (2016).
[Crossref]

Darzacq, X.

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

Deerinck, T. J.

H. D. Ou, S. Phan, T. J. Deerinck, A. Thor, M. H. Ellisman, and C. C. O’Shea, Science 357, eaag0025 (2017).
[Crossref]

Dong, B.

B. Dong, L. M. Almassalha, B. T. Soetikno, J. E. Chandler, B. E. Urban, C. Sun, H. F. Zhang, and V. Backman, Opt. Express 25, 7929 (2017).
[Crossref]

B. Dong, L. M. Almassalha, Y. Stypula-Cyrus, B. E. Urban, J. E. Chandler, C. Sun, H. F. Zhang, and V. Backman, Proc. Natl. Acad. Sci. USA 113, 9716 (2016).
[Crossref]

B. Dong, L. Almassalha, B. E. Urban, S. Khuon, T.-L. Chew, V. Backman, C. Sun, and H. F. Zhang, Nat. Commun. 7, 12290 (2016).
[Crossref]

Duboule, D.

P. J. Fabre, A. Benke, S. Manley, and D. Duboule, Cold Spring Harbor Symposia on Quantitative Biology (Cold Spring Harbor Laboratory, 2015), pp. 9–16.

Ellis, R. J.

R. J. Ellis and A. P. Minton, Nature 425, 27 (2003).
[Crossref]

Ellisman, M. H.

H. D. Ou, S. Phan, T. J. Deerinck, A. Thor, M. H. Ellisman, and C. C. O’Shea, Science 357, eaag0025 (2017).
[Crossref]

Fabre, P. J.

P. J. Fabre, A. Benke, S. Manley, and D. Duboule, Cold Spring Harbor Symposia on Quantitative Biology (Cold Spring Harbor Laboratory, 2015), pp. 9–16.

Fonseka, C. Y.

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Fourré, N.

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

Griffiths, C.

R. Henriques, C. Griffiths, E. Hesper Rego, and M. M. Mhlanga, Biopolymers 95, 322 (2011).
[Crossref]

Hagen, G. M.

M. Ovesný, P. Křížek, J. Borkovec, Z. Švindrych, and G. M. Hagen, Bioinformatics 30, 2389 (2014).
[Crossref]

Hanson, B. L.

J. M. Harp, B. L. Hanson, D. E. Timm, and G. J. Bunick, Acta Crystallogr. Sect. D 56, 1513 (2000).
[Crossref]

Harp, J. M.

J. M. Harp, B. L. Hanson, D. E. Timm, and G. J. Bunick, Acta Crystallogr. Sect. D 56, 1513 (2000).
[Crossref]

Heliot, L.

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

Henriques, R.

R. Henriques, C. Griffiths, E. Hesper Rego, and M. M. Mhlanga, Biopolymers 95, 322 (2011).
[Crossref]

Hesper Rego, E.

R. Henriques, C. Griffiths, E. Hesper Rego, and M. M. Mhlanga, Biopolymers 95, 322 (2011).
[Crossref]

Joyce, E. F.

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Jungmann, R.

J. Schnitzbauer, M. T. Strauss, T. Schlichthaerle, F. Schueder, and R. Jungmann, Nat. Protoc. 12, 1198 (2017).
[Crossref]

Khuon, S.

B. Dong, L. Almassalha, B. E. Urban, S. Khuon, T.-L. Chew, V. Backman, C. Sun, and H. F. Zhang, Nat. Commun. 7, 12290 (2016).
[Crossref]

Krížek, P.

M. Ovesný, P. Křížek, J. Borkovec, Z. Švindrych, and G. M. Hagen, Bioinformatics 30, 2389 (2014).
[Crossref]

Li, J. B.

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Luger, K.

K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent, and T. J. Richmond, Nature 389, 251 (1997).
[Crossref]

Mäder, A. W.

K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent, and T. J. Richmond, Nature 389, 251 (1997).
[Crossref]

Manley, S.

P. J. Fabre, A. Benke, S. Manley, and D. Duboule, Cold Spring Harbor Symposia on Quantitative Biology (Cold Spring Harbor Laboratory, 2015), pp. 9–16.

McCole, R. B.

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Mhlanga, M. M.

R. Henriques, C. Griffiths, E. Hesper Rego, and M. M. Mhlanga, Biopolymers 95, 322 (2011).
[Crossref]

Minton, A. P.

R. J. Ellis and A. P. Minton, Nature 425, 27 (2003).
[Crossref]

Moffitt, J. R.

S. Wang, J.-H. Su, B. J. Beliveau, B. Bintu, J. R. Moffitt, C.-T. Wu, and X. Zhuang, Science 353, 598 (2016).
[Crossref]

O’Shea, C. C.

H. D. Ou, S. Phan, T. J. Deerinck, A. Thor, M. H. Ellisman, and C. C. O’Shea, Science 357, eaag0025 (2017).
[Crossref]

Ou, H. D.

H. D. Ou, S. Phan, T. J. Deerinck, A. Thor, M. H. Ellisman, and C. C. O’Shea, Science 357, eaag0025 (2017).
[Crossref]

Ovesný, M.

M. Ovesný, P. Křížek, J. Borkovec, Z. Švindrych, and G. M. Hagen, Bioinformatics 30, 2389 (2014).
[Crossref]

Phan, S.

H. D. Ou, S. Phan, T. J. Deerinck, A. Thor, M. H. Ellisman, and C. C. O’Shea, Science 357, eaag0025 (2017).
[Crossref]

Richard, E.

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

Richmond, R. K.

K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent, and T. J. Richmond, Nature 389, 251 (1997).
[Crossref]

Richmond, T. J.

K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent, and T. J. Richmond, Nature 389, 251 (1997).
[Crossref]

Sargent, D. F.

K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent, and T. J. Richmond, Nature 389, 251 (1997).
[Crossref]

Sarikaya, M.

H. Yokota, J. Sunwoo, M. Sarikaya, G. van den Engh, and R. Aebersold, Anal. Chem. 71, 4418 (1999).
[Crossref]

Schlichthaerle, T.

J. Schnitzbauer, M. T. Strauss, T. Schlichthaerle, F. Schueder, and R. Jungmann, Nat. Protoc. 12, 1198 (2017).
[Crossref]

Schnitzbauer, J.

J. Schnitzbauer, M. T. Strauss, T. Schlichthaerle, F. Schueder, and R. Jungmann, Nat. Protoc. 12, 1198 (2017).
[Crossref]

Schueder, F.

J. Schnitzbauer, M. T. Strauss, T. Schlichthaerle, F. Schueder, and R. Jungmann, Nat. Protoc. 12, 1198 (2017).
[Crossref]

Senaratne, T. N.

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Soetikno, B. T.

Spriet, C.

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

Strauss, M. T.

J. Schnitzbauer, M. T. Strauss, T. Schlichthaerle, F. Schueder, and R. Jungmann, Nat. Protoc. 12, 1198 (2017).
[Crossref]

Stypula-Cyrus, Y.

B. Dong, L. M. Almassalha, Y. Stypula-Cyrus, B. E. Urban, J. E. Chandler, C. Sun, H. F. Zhang, and V. Backman, Proc. Natl. Acad. Sci. USA 113, 9716 (2016).
[Crossref]

Su, J.-H.

S. Wang, J.-H. Su, B. J. Beliveau, B. Bintu, J. R. Moffitt, C.-T. Wu, and X. Zhuang, Science 353, 598 (2016).
[Crossref]

Sun, C.

B. Dong, L. M. Almassalha, B. T. Soetikno, J. E. Chandler, B. E. Urban, C. Sun, H. F. Zhang, and V. Backman, Opt. Express 25, 7929 (2017).
[Crossref]

B. Dong, L. M. Almassalha, Y. Stypula-Cyrus, B. E. Urban, J. E. Chandler, C. Sun, H. F. Zhang, and V. Backman, Proc. Natl. Acad. Sci. USA 113, 9716 (2016).
[Crossref]

B. Dong, L. Almassalha, B. E. Urban, S. Khuon, T.-L. Chew, V. Backman, C. Sun, and H. F. Zhang, Nat. Commun. 7, 12290 (2016).
[Crossref]

Sunwoo, J.

H. Yokota, J. Sunwoo, M. Sarikaya, G. van den Engh, and R. Aebersold, Anal. Chem. 71, 4418 (1999).
[Crossref]

Švindrych, Z.

M. Ovesný, P. Křížek, J. Borkovec, Z. Švindrych, and G. M. Hagen, Bioinformatics 30, 2389 (2014).
[Crossref]

Thor, A.

H. D. Ou, S. Phan, T. J. Deerinck, A. Thor, M. H. Ellisman, and C. C. O’Shea, Science 357, eaag0025 (2017).
[Crossref]

Timm, D. E.

J. M. Harp, B. L. Hanson, D. E. Timm, and G. J. Bunick, Acta Crystallogr. Sect. D 56, 1513 (2000).
[Crossref]

Trinel, D.

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

Urban, B. E.

B. Dong, L. M. Almassalha, B. T. Soetikno, J. E. Chandler, B. E. Urban, C. Sun, H. F. Zhang, and V. Backman, Opt. Express 25, 7929 (2017).
[Crossref]

B. Dong, L. M. Almassalha, Y. Stypula-Cyrus, B. E. Urban, J. E. Chandler, C. Sun, H. F. Zhang, and V. Backman, Proc. Natl. Acad. Sci. USA 113, 9716 (2016).
[Crossref]

B. Dong, L. Almassalha, B. E. Urban, S. Khuon, T.-L. Chew, V. Backman, C. Sun, and H. F. Zhang, Nat. Commun. 7, 12290 (2016).
[Crossref]

van den Engh, G.

H. Yokota, J. Sunwoo, M. Sarikaya, G. van den Engh, and R. Aebersold, Anal. Chem. 71, 4418 (1999).
[Crossref]

Vandenbunder, B.

E. Richard, S. Causse, C. Spriet, N. Fourré, D. Trinel, X. Darzacq, B. Vandenbunder, and L. Heliot, Photochem. Photobiol. 87, 256 (2011).
[Crossref]

Wang, S.

S. Wang, J.-H. Su, B. J. Beliveau, B. Bintu, J. R. Moffitt, C.-T. Wu, and X. Zhuang, Science 353, 598 (2016).
[Crossref]

Williams, B. R.

B. J. Beliveau, E. F. Joyce, N. Apostolopoulos, F. Yilmaz, C. Y. Fonseka, R. B. McCole, Y. Chang, J. B. Li, T. N. Senaratne, and B. R. Williams, Proc. Natl. Acad. Sci. USA 109, 21301 (2012).
[Crossref]

Wu, C.-T.

S. Wang, J.-H. Su, B. J. Beliveau, B. Bintu, J. R. Moffitt, C.-T. Wu, and X. Zhuang, Science 353, 598 (2016).
[Crossref]

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Figures (5)

Fig. 1.
Fig. 1. System schematic. Fluorescent images were collected by a high numerical aperture objective lens and sent to a Czerny–Turner monochromator, where the zero- and first-order images are read separately and simultaneously with an EMCCD.
Fig. 2.
Fig. 2. (a) Photon counts and emission spectra centroids associated with 100 blinking events for unlabeled 20 bp sequences of poly-G, poly-A, poly-T, and poly-C. (b) Spectral heterogeneity of unlabeled poly-DNA molecules. (c) and (d) Emission spectra of individual stochastic localization at two neighboring spots indicated by blue and red dots in (b). The emission events can be separated clearly according to their emission properties, indicating they are from two different emitters.
Fig. 3.
Fig. 3. Flow chart of SR algorithm. Conventional PLM reconstruction was performed in ThuderSTORM. Using the SR algorithm, emission events that belong to the same molecule were added (merged) to improve the accuracy of emitter localization.
Fig. 4.
Fig. 4. (a) Wide-field image of 20-mer poly-DNA, (b) STORM reconstruction of 20-mer poly-DNA, (c) enlarged view of two 20-mer poly-DNA molecules, (d) after SR the two 20-mer poly-DNA molecules are separable, and (e) the FWHM of each individual molecule is shown to be 6.2 nm, where the molecules are shown to be spaced 16 nm apart.
Fig. 5.
Fig. 5. (a) Wide-field fluorescence image of Hoechst stained DNA fiber, (b) STORM reconstruction of DNA fiber using 532 nm illumination, (c) STORM reconstruction of DNA fiber after applying SR algorithm, (d) enlarged view of selection shown in (b), (e) enlarged view of selection shown in (c), (f) an image acquired by AFM of a separate single DNA fiber, (g) comparison of resolution between traditional PLM and SICLON with SR shows a four times resolution enhancement, and (h) AFM reveals the ground truth width of the fiber is estimated to be 4.1 nm.

Equations (1)

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α 2 π 0 { [ erf ( x + σ sin g l e σ multiple 2 ) erf ( x 2 ) ] exp ( x 2 2 ) } d x .

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