Abstract

We consider multi-modal four-wave mixing microscopies to be ideal tools for the in vivo study of carotenoid distributions within the important biofuel microalgae Haematococcus pluvialis. We show that hyperspectral coherent anti-Stokes Raman scattering (CARS) microscopy generates non-invasive, quantitative real-time concentrations maps of intracellular carotenoid distributions in live algae.

© 2014 Optical Society of America

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  1. W. M. Tolles, J. W. Nibler, J. R. McDonald, and A. B. Harvey, “A Review of the Theory and Application of Coherent Anti-Stokes Raman Spectroscopy (CARS),” Appl. Spectrosc. 31(4), 253–271 (1977).
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  5. C. L. Evans and X. S. Xie, “Coherent Anti-Stokes Raman Scattering Microscopy: Chemical Imaging for Biology and Medicine,” Annu Rev Anal Chem (Palo Alto Calif) 1(1), 883–909 (2008).
    [Crossref] [PubMed]
  6. Y. Wang, C.-Y. Lin, A. Nikolaenko, V. Raghunathan, and E. O. Potma, “Four-wave mixing microscopy of nanostructures,” Adv. Opt. Photon. 3(1), 1 (2011).
    [Crossref]
  7. J. Renger, R. Quidant, N. v. Hulst, and L. Novotny, “Surface-Enhanced Nonlinear Four-Wave Mixing,” Phys. Rev. Lett. 104, 046803 (2010).
  8. M. Danckwerts and L. Novotny, “Optical Frequency Mixing at Coupled Gold Nanoparticles,” Phys. Rev. Lett. 98(2), 026104 (2007).
    [Crossref] [PubMed]
  9. L. Huang and J.-X. Cheng, “Nonlinear Optical Microscopy of Single Nanostructures,” Annu. Rev. Mater. Res. 43(1), 213–236 (2013).
    [Crossref]
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    [Crossref]
  13. L. Fan, A. Vonshak, A. Zarka, and S. Boussiba, “Does astaxanthin protect Haematococcus against light damage?” Z. Naturforsch., C, J. Biosci. 53(1-2), 93–100 (1998).
    [PubMed]
  14. K. Grünewald, J. Hirschberg, and C. Hagen, “Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis,” J. Biol. Chem. 276(8), 6023–6029 (2001).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [PubMed]
  17. J.-P. Yuan, J. Peng, K. Yin, and J.-H. Wang, “Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae,” Mol. Nutr. Food Res. 55(1), 150–165 (2011).
    [Crossref] [PubMed]
  18. M. C. Damiani, C. A. Popovich, D. Constenla, and P. I. Leonardi, “Lipid analysis in Haematococcuspluvialis to assess its potential use as a biodiesel feedstock,” Bioresour. Technol. 101(11), 3801–3807 (2010).
    [Crossref] [PubMed]
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    [Crossref]
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    [Crossref]
  21. A. Kaczor, K. Turnau, and M. Baranska, “In situ Raman imaging of astaxanthin in a single microalgal cell,” Analyst (Lond.) 136(6), 1109–1112 (2011).
    [Crossref] [PubMed]
  22. A. M. Collins, H. D. T. Jones, D. Han, Q. Hu, T. E. Beechem, and J. A. Timlin, “Carotenoid Distribution in Living Cells of Haematococcus pluvialis (Chlorophyceae),” PLoS ONE 6(9), e24302 (2011).
    [Crossref] [PubMed]
  23. M. Wayama, S. Ota, H. Matsuura, N. Nango, A. Hirata, and S. Kawano, “Three-Dimensional Ultrastructural Study of Oil and Astaxanthin Accumulation during Encystment in the Green Alga Haematococcus pluvialis,” PLoS ONE 8(1), e53618 (2013).
    [Crossref] [PubMed]
  24. C. Brackmann, A. Bengtsson, M. L. Alminger, U. Svanberg, and A. Enejder, “Visualization of beta-carotene and starch granules in plant cells using CARS and SHG microscopy,” J. Ram 42(4Spec.), 586–592 (2011).
    [Crossref]
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    [Crossref]
  27. X. N. He, J. Allen, P. N. Black, T. Baldacchini, X. Huang, H. Huang, L. Jiang, and Y. F. Lu, “Coherent anti-Stokes Raman scattering and spontaneous Raman spectroscopy and microscopy of microalgae with nitrogen depletion,” Biomed. Opt. Express 3(11), 2896–2906 (2012).
    [Crossref] [PubMed]
  28. P. Mahou, N. Olivier, G. Labroille, L. Duloquin, J.-M. Sintes, N. Peyriéras, R. Legouis, D. Débarre, and E. Beaurepaire, “Combined third-harmonic generation and four-wave mixing microscopy of tissues and embryos,” Biomed. Opt. Express 2(10), 2837–2849 (2011).
    [Crossref] [PubMed]
  29. P. D. Maker and R. W. Terhune, “Study of Optical Effects Due to an Induced Polarization Third Order in the Electric Field Strength,” Phys. Rev. 137(3A), A801–A818 (1965).
    [Crossref]
  30. M. Cui, B. R. Bachler, and J. P. Ogilvie, “Comparing coherent and spontaneous Raman scattering under biological imaging conditions,” Opt. Lett. 34(6), 773–775 (2009).
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  31. J.-X. Cheng and X. S. Xie, “Coherent Anti-Stokes Raman Scattering Microscopy: Instrumentation, Theory, and Applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
    [Crossref]
  32. J.-X. Cheng, L. D. Book, and X. S. Xie, “Polarization coherent anti-Stokes Raman scattering microscopy,” Opt. Lett. 26(17), 1341–1343 (2001).
    [Crossref] [PubMed]
  33. E. O. Potma, C. L. Evans, and X. S. Xie, “Heterodyne coherent anti-Stokes Raman scattering (CARS) imaging,” Opt. Lett. 31(2), 241–243 (2006).
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  34. Y. Liu, Y. J. Lee, and M. T. Cicerone, “Broadband CARS spectral phase retrieval using a time-domain Kramers-Kronig transform,” Opt. Lett. 34(9), 1363–1365 (2009).
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  35. E. M. Vartiainen, H. A. Rinia, M. Müller, and M. Bonn, “Direct extraction of Raman line-shapes from congested CARS spectra,” Opt. Express 14(8), 3622–3630 (2006).
    [Crossref] [PubMed]
  36. F. Masia, A. Glen, P. Stephens, P. Borri, and W. Langbein, “Quantitative Chemical Imaging and Unsupervised Analysis Using Hyperspectral Coherent Anti-Stokes Raman Scattering Microscopy,” Anal. Chem. 85(22), 10820–10828 (2013).
    [Crossref] [PubMed]
  37. A. F. Pegoraro, A. D. Slepkov, A. R. Ridsdale, D. J. Moffatt, and A. Stolow, “Hyperspectral multimodal CARS microscopy in the fingerprint region,” J. Biophotonics 7(1-2), 49–58 (2014).
    [Crossref] [PubMed]
  38. A. D. Slepkov, A. M. Barlow, A. R. Ridsdale, P. J. McGinn, and A. Stolow, “In vivo hyperspectral CARS and FWM microscopy of carotenoid accumulation in H. Pluvialis,” Proc. SPIE 8937, Multimodal Biomedical Imaging IX, 893709 (2014).
  39. T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85(1), 25–27 (2004).
    [Crossref]
  40. I. Rocha-Mendoza, W. Langbein, and P. Borri, “Coherent anti-Stokes Raman microspectroscopy using spectral focusing with glass dispersion,” Appl. Phys. Lett. 93(20), 201103 (2008).
    [Crossref]
  41. R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
    [Crossref] [PubMed]
  42. Y. Fu, H. Wang, R. Shi, and J.-X. Cheng, “Characterization of photodamage in coherent anti-Stokes Raman scattering microscopy,” Opt. Express 14(9), 3942–3951 (2006).
    [Crossref] [PubMed]
  43. A. G. Christophersen, H. Jun, K. Jørgensen, and L. H. Skibsted, “Photobleaching of astaxanthin and canthaxanthin,” Z. Lebensm. Unters. Forsch. 192(5), 433–439 (1991).
  44. H.-M. Chen and S. P. Meyers, “A rapid quantitative method for determination of astaxanthin pigment concentration in oil extracts,” J. Am. Oil Chem. Soc. 61(6), 1045–1047 (1984).
    [Crossref]
  45. L. Rimai, M. E. Heyde, and D. Gill, “Vibrational spectra of some carotenoids and related linear polyenes. Raman spectroscopic study,” J. Am. Chem. Soc. 95(14), 4493–4501 (1973).
    [Crossref] [PubMed]
  46. Y. Koyama, M. Kuki, P. O. Andersson, and T. Gillbro, “Singlet Excited States and the Light-Harvesting Function of Carotenoids in Bacterial Photosynthesis,” Photochem. Photobiol. 63(3), 243–256 (1996).
    [Crossref]

2014 (2)

A. F. Pegoraro, A. D. Slepkov, A. R. Ridsdale, D. J. Moffatt, and A. Stolow, “Hyperspectral multimodal CARS microscopy in the fingerprint region,” J. Biophotonics 7(1-2), 49–58 (2014).
[Crossref] [PubMed]

A. D. Slepkov, A. M. Barlow, A. R. Ridsdale, P. J. McGinn, and A. Stolow, “In vivo hyperspectral CARS and FWM microscopy of carotenoid accumulation in H. Pluvialis,” Proc. SPIE 8937, Multimodal Biomedical Imaging IX, 893709 (2014).

2013 (4)

M. Wayama, S. Ota, H. Matsuura, N. Nango, A. Hirata, and S. Kawano, “Three-Dimensional Ultrastructural Study of Oil and Astaxanthin Accumulation during Encystment in the Green Alga Haematococcus pluvialis,” PLoS ONE 8(1), e53618 (2013).
[Crossref] [PubMed]

A. Dementjev and J. Kostkevičiene, “Applying the method of Coherent Anti-stokes Raman microscopy for imaging of carotenoids in microalgae and cyanobacteria,” J. Ram 44(7Spec.), 973–979 (2013).
[Crossref]

L. Huang and J.-X. Cheng, “Nonlinear Optical Microscopy of Single Nanostructures,” Annu. Rev. Mater. Res. 43(1), 213–236 (2013).
[Crossref]

F. Masia, A. Glen, P. Stephens, P. Borri, and W. Langbein, “Quantitative Chemical Imaging and Unsupervised Analysis Using Hyperspectral Coherent Anti-Stokes Raman Scattering Microscopy,” Anal. Chem. 85(22), 10820–10828 (2013).
[Crossref] [PubMed]

2012 (3)

K. Tominaga, N. Hongo, M. Karato, and E. Yamashita, “Cosmetic benefits of astaxanthin on humans subjects,” Acta Biochim. Pol. 59(1), 43–47 (2012).
[PubMed]

X. N. He, J. Allen, P. N. Black, T. Baldacchini, X. Huang, H. Huang, L. Jiang, and Y. F. Lu, “Coherent anti-Stokes Raman scattering and spontaneous Raman spectroscopy and microscopy of microalgae with nitrogen depletion,” Biomed. Opt. Express 3(11), 2896–2906 (2012).
[Crossref] [PubMed]

Z. Pilát, S. Bernatová, J. Ježek, M. Šerý, O. Samek, P. Zemánek, L. Nedbal, and M. Trtílek, “Raman microspectroscopy of algal lipid bodies: β-carotene quantification,” J. Appl. Phycol. 24(3), 541–546 (2012).
[Crossref]

2011 (6)

A. Kaczor, K. Turnau, and M. Baranska, “In situ Raman imaging of astaxanthin in a single microalgal cell,” Analyst (Lond.) 136(6), 1109–1112 (2011).
[Crossref] [PubMed]

A. M. Collins, H. D. T. Jones, D. Han, Q. Hu, T. E. Beechem, and J. A. Timlin, “Carotenoid Distribution in Living Cells of Haematococcus pluvialis (Chlorophyceae),” PLoS ONE 6(9), e24302 (2011).
[Crossref] [PubMed]

C. Brackmann, A. Bengtsson, M. L. Alminger, U. Svanberg, and A. Enejder, “Visualization of beta-carotene and starch granules in plant cells using CARS and SHG microscopy,” J. Ram 42(4Spec.), 586–592 (2011).
[Crossref]

P. Mahou, N. Olivier, G. Labroille, L. Duloquin, J.-M. Sintes, N. Peyriéras, R. Legouis, D. Débarre, and E. Beaurepaire, “Combined third-harmonic generation and four-wave mixing microscopy of tissues and embryos,” Biomed. Opt. Express 2(10), 2837–2849 (2011).
[Crossref] [PubMed]

J.-P. Yuan, J. Peng, K. Yin, and J.-H. Wang, “Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae,” Mol. Nutr. Food Res. 55(1), 150–165 (2011).
[Crossref] [PubMed]

Y. Wang, C.-Y. Lin, A. Nikolaenko, V. Raghunathan, and E. O. Potma, “Four-wave mixing microscopy of nanostructures,” Adv. Opt. Photon. 3(1), 1 (2011).
[Crossref]

2010 (2)

J. Renger, R. Quidant, N. v. Hulst, and L. Novotny, “Surface-Enhanced Nonlinear Four-Wave Mixing,” Phys. Rev. Lett. 104, 046803 (2010).

M. C. Damiani, C. A. Popovich, D. Constenla, and P. I. Leonardi, “Lipid analysis in Haematococcuspluvialis to assess its potential use as a biodiesel feedstock,” Bioresour. Technol. 101(11), 3801–3807 (2010).
[Crossref] [PubMed]

2009 (4)

2008 (2)

I. Rocha-Mendoza, W. Langbein, and P. Borri, “Coherent anti-Stokes Raman microspectroscopy using spectral focusing with glass dispersion,” Appl. Phys. Lett. 93(20), 201103 (2008).
[Crossref]

C. L. Evans and X. S. Xie, “Coherent Anti-Stokes Raman Scattering Microscopy: Chemical Imaging for Biology and Medicine,” Annu Rev Anal Chem (Palo Alto Calif) 1(1), 883–909 (2008).
[Crossref] [PubMed]

2007 (1)

M. Danckwerts and L. Novotny, “Optical Frequency Mixing at Coupled Gold Nanoparticles,” Phys. Rev. Lett. 98(2), 026104 (2007).
[Crossref] [PubMed]

2006 (4)

2004 (3)

T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85(1), 25–27 (2004).
[Crossref]

J.-X. Cheng and X. S. Xie, “Coherent Anti-Stokes Raman Scattering Microscopy: Instrumentation, Theory, and Applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
[Crossref]

E. O. Potma and X. S. Xie, “CARS microscopy for biology and medicine,” Opt. Photonics News 15(11), 40–45 (2004).
[Crossref]

2003 (1)

M. Guerin, M. E. Huntley, and M. Olaizola, “Haematococcus astaxanthin: applications for human health and nutrition,” Trends Biotechnol. 21(5), 210–216 (2003).
[Crossref] [PubMed]

2001 (2)

J.-X. Cheng, L. D. Book, and X. S. Xie, “Polarization coherent anti-Stokes Raman scattering microscopy,” Opt. Lett. 26(17), 1341–1343 (2001).
[Crossref] [PubMed]

K. Grünewald, J. Hirschberg, and C. Hagen, “Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis,” J. Biol. Chem. 276(8), 6023–6029 (2001).
[Crossref] [PubMed]

2000 (1)

S. Boussiba, “Carotenogenesis in the green alga Haematococcus pluvialis: Cellular physiology and stress response,” Physiol. Plant. 108(2), 111–117 (2000).
[Crossref]

1999 (1)

A. Zumbusch, G. R. Holtom, and X. S. Xie, “Three-dimensional vibrational imaging by coherent anti-Stokes Raman scattering,” Phys. Rev. Lett. 82(20), 4142–4145 (1999).
[Crossref]

1998 (1)

L. Fan, A. Vonshak, A. Zarka, and S. Boussiba, “Does astaxanthin protect Haematococcus against light damage?” Z. Naturforsch., C, J. Biosci. 53(1-2), 93–100 (1998).
[PubMed]

1996 (1)

Y. Koyama, M. Kuki, P. O. Andersson, and T. Gillbro, “Singlet Excited States and the Light-Harvesting Function of Carotenoids in Bacterial Photosynthesis,” Photochem. Photobiol. 63(3), 243–256 (1996).
[Crossref]

1993 (1)

C. Castiglioni, M. Del Zoppo, and G. Zerbi, “Vibrational Raman spectroscopy of polyconjugated organic oligomers and polymers,” J. Ram 24(8Spec.), 485–494 (1993).
[Crossref]

1991 (1)

A. G. Christophersen, H. Jun, K. Jørgensen, and L. H. Skibsted, “Photobleaching of astaxanthin and canthaxanthin,” Z. Lebensm. Unters. Forsch. 192(5), 433–439 (1991).

1984 (1)

H.-M. Chen and S. P. Meyers, “A rapid quantitative method for determination of astaxanthin pigment concentration in oil extracts,” J. Am. Oil Chem. Soc. 61(6), 1045–1047 (1984).
[Crossref]

1977 (1)

1973 (1)

L. Rimai, M. E. Heyde, and D. Gill, “Vibrational spectra of some carotenoids and related linear polyenes. Raman spectroscopic study,” J. Am. Chem. Soc. 95(14), 4493–4501 (1973).
[Crossref] [PubMed]

1965 (1)

P. D. Maker and R. W. Terhune, “Study of Optical Effects Due to an Induced Polarization Third Order in the Electric Field Strength,” Phys. Rev. 137(3A), A801–A818 (1965).
[Crossref]

1954 (2)

M. R. Droop, “Conditions governing haematochrome formation and loss in the alga haematocuccus pluvialis flotow,” Arch. Mikrobiol. 20(4), 391–397 (1954).
[Crossref] [PubMed]

T. W. Goodwin and M. Jamikorn, “Studies in carotenogenesis. 11. Carotenoid synthesis in the alga Haematococcus pluvialis,” Biochem. J. 57(3), 376–381 (1954).
[PubMed]

Allen, J.

Alminger, M. L.

C. Brackmann, A. Bengtsson, M. L. Alminger, U. Svanberg, and A. Enejder, “Visualization of beta-carotene and starch granules in plant cells using CARS and SHG microscopy,” J. Ram 42(4Spec.), 586–592 (2011).
[Crossref]

Andersson, P. O.

Y. Koyama, M. Kuki, P. O. Andersson, and T. Gillbro, “Singlet Excited States and the Light-Harvesting Function of Carotenoids in Bacterial Photosynthesis,” Photochem. Photobiol. 63(3), 243–256 (1996).
[Crossref]

Bachler, B. R.

Baldacchini, T.

Baranska, M.

A. Kaczor, K. Turnau, and M. Baranska, “In situ Raman imaging of astaxanthin in a single microalgal cell,” Analyst (Lond.) 136(6), 1109–1112 (2011).
[Crossref] [PubMed]

Barlow, A. M.

A. D. Slepkov, A. M. Barlow, A. R. Ridsdale, P. J. McGinn, and A. Stolow, “In vivo hyperspectral CARS and FWM microscopy of carotenoid accumulation in H. Pluvialis,” Proc. SPIE 8937, Multimodal Biomedical Imaging IX, 893709 (2014).

Beaurepaire, E.

Beechem, T. E.

A. M. Collins, H. D. T. Jones, D. Han, Q. Hu, T. E. Beechem, and J. A. Timlin, “Carotenoid Distribution in Living Cells of Haematococcus pluvialis (Chlorophyceae),” PLoS ONE 6(9), e24302 (2011).
[Crossref] [PubMed]

Bengtsson, A.

C. Brackmann, A. Bengtsson, M. L. Alminger, U. Svanberg, and A. Enejder, “Visualization of beta-carotene and starch granules in plant cells using CARS and SHG microscopy,” J. Ram 42(4Spec.), 586–592 (2011).
[Crossref]

Bernatová, S.

Z. Pilát, S. Bernatová, J. Ježek, M. Šerý, O. Samek, P. Zemánek, L. Nedbal, and M. Trtílek, “Raman microspectroscopy of algal lipid bodies: β-carotene quantification,” J. Appl. Phycol. 24(3), 541–546 (2012).
[Crossref]

Black, P. N.

Blais, D. R.

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
[Crossref] [PubMed]

Bonn, M.

Book, L. D.

Borri, P.

F. Masia, A. Glen, P. Stephens, P. Borri, and W. Langbein, “Quantitative Chemical Imaging and Unsupervised Analysis Using Hyperspectral Coherent Anti-Stokes Raman Scattering Microscopy,” Anal. Chem. 85(22), 10820–10828 (2013).
[Crossref] [PubMed]

I. Rocha-Mendoza, W. Langbein, and P. Borri, “Coherent anti-Stokes Raman microspectroscopy using spectral focusing with glass dispersion,” Appl. Phys. Lett. 93(20), 201103 (2008).
[Crossref]

Boussiba, S.

S. Boussiba, “Carotenogenesis in the green alga Haematococcus pluvialis: Cellular physiology and stress response,” Physiol. Plant. 108(2), 111–117 (2000).
[Crossref]

L. Fan, A. Vonshak, A. Zarka, and S. Boussiba, “Does astaxanthin protect Haematococcus against light damage?” Z. Naturforsch., C, J. Biosci. 53(1-2), 93–100 (1998).
[PubMed]

Brackmann, C.

C. Brackmann, A. Bengtsson, M. L. Alminger, U. Svanberg, and A. Enejder, “Visualization of beta-carotene and starch granules in plant cells using CARS and SHG microscopy,” J. Ram 42(4Spec.), 586–592 (2011).
[Crossref]

Castiglioni, C.

C. Castiglioni, M. Del Zoppo, and G. Zerbi, “Vibrational Raman spectroscopy of polyconjugated organic oligomers and polymers,” J. Ram 24(8Spec.), 485–494 (1993).
[Crossref]

Chen, H.-M.

H.-M. Chen and S. P. Meyers, “A rapid quantitative method for determination of astaxanthin pigment concentration in oil extracts,” J. Am. Oil Chem. Soc. 61(6), 1045–1047 (1984).
[Crossref]

Cheng, J.-X.

L. Huang and J.-X. Cheng, “Nonlinear Optical Microscopy of Single Nanostructures,” Annu. Rev. Mater. Res. 43(1), 213–236 (2013).
[Crossref]

Y. Fu, H. Wang, R. Shi, and J.-X. Cheng, “Characterization of photodamage in coherent anti-Stokes Raman scattering microscopy,” Opt. Express 14(9), 3942–3951 (2006).
[Crossref] [PubMed]

J.-X. Cheng and X. S. Xie, “Coherent Anti-Stokes Raman Scattering Microscopy: Instrumentation, Theory, and Applications,” J. Phys. Chem. B 108(3), 827–840 (2004).
[Crossref]

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A. M. Collins, H. D. T. Jones, D. Han, Q. Hu, T. E. Beechem, and J. A. Timlin, “Carotenoid Distribution in Living Cells of Haematococcus pluvialis (Chlorophyceae),” PLoS ONE 6(9), e24302 (2011).
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Harvey, A. B.

He, X. N.

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T. Hellerer, A. M. K. Enejder, and A. Zumbusch, “Spectral focusing: High spectral resolution spectroscopy with broad-bandwidth laser pulses,” Appl. Phys. Lett. 85(1), 25–27 (2004).
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Heyde, M. E.

L. Rimai, M. E. Heyde, and D. Gill, “Vibrational spectra of some carotenoids and related linear polyenes. Raman spectroscopic study,” J. Am. Chem. Soc. 95(14), 4493–4501 (1973).
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M. Wayama, S. Ota, H. Matsuura, N. Nango, A. Hirata, and S. Kawano, “Three-Dimensional Ultrastructural Study of Oil and Astaxanthin Accumulation during Encystment in the Green Alga Haematococcus pluvialis,” PLoS ONE 8(1), e53618 (2013).
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K. Grünewald, J. Hirschberg, and C. Hagen, “Ketocarotenoid biosynthesis outside of plastids in the unicellular green alga Haematococcus pluvialis,” J. Biol. Chem. 276(8), 6023–6029 (2001).
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K. Tominaga, N. Hongo, M. Karato, and E. Yamashita, “Cosmetic benefits of astaxanthin on humans subjects,” Acta Biochim. Pol. 59(1), 43–47 (2012).
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Hu, Q.

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Huang, L.

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Huang, X.

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Huntley, M. E.

M. Guerin, M. E. Huntley, and M. Olaizola, “Haematococcus astaxanthin: applications for human health and nutrition,” Trends Biotechnol. 21(5), 210–216 (2003).
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Jamikorn, M.

T. W. Goodwin and M. Jamikorn, “Studies in carotenogenesis. 11. Carotenoid synthesis in the alga Haematococcus pluvialis,” Biochem. J. 57(3), 376–381 (1954).
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Ježek, J.

Z. Pilát, S. Bernatová, J. Ježek, M. Šerý, O. Samek, P. Zemánek, L. Nedbal, and M. Trtílek, “Raman microspectroscopy of algal lipid bodies: β-carotene quantification,” J. Appl. Phycol. 24(3), 541–546 (2012).
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Jia, Y.

Jiang, L.

Jones, H. D. T.

A. M. Collins, H. D. T. Jones, D. Han, Q. Hu, T. E. Beechem, and J. A. Timlin, “Carotenoid Distribution in Living Cells of Haematococcus pluvialis (Chlorophyceae),” PLoS ONE 6(9), e24302 (2011).
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Jørgensen, K.

A. G. Christophersen, H. Jun, K. Jørgensen, and L. H. Skibsted, “Photobleaching of astaxanthin and canthaxanthin,” Z. Lebensm. Unters. Forsch. 192(5), 433–439 (1991).

Jun, H.

A. G. Christophersen, H. Jun, K. Jørgensen, and L. H. Skibsted, “Photobleaching of astaxanthin and canthaxanthin,” Z. Lebensm. Unters. Forsch. 192(5), 433–439 (1991).

Kaczor, A.

A. Kaczor, K. Turnau, and M. Baranska, “In situ Raman imaging of astaxanthin in a single microalgal cell,” Analyst (Lond.) 136(6), 1109–1112 (2011).
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H. Kano and H. Hamaguchi, “Vibrationally resonant imaging of a single living cell by supercontinuum-based multiplex coherent anti-Stokes Raman scattering microspectroscopy,” Chem. Lett. 35, 1124–1125 (2006).
[Crossref]

Karato, M.

K. Tominaga, N. Hongo, M. Karato, and E. Yamashita, “Cosmetic benefits of astaxanthin on humans subjects,” Acta Biochim. Pol. 59(1), 43–47 (2012).
[PubMed]

Kawano, S.

M. Wayama, S. Ota, H. Matsuura, N. Nango, A. Hirata, and S. Kawano, “Three-Dimensional Ultrastructural Study of Oil and Astaxanthin Accumulation during Encystment in the Green Alga Haematococcus pluvialis,” PLoS ONE 8(1), e53618 (2013).
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Kennedy, D. C.

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
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Kostkeviciene, J.

A. Dementjev and J. Kostkevičiene, “Applying the method of Coherent Anti-stokes Raman microscopy for imaging of carotenoids in microalgae and cyanobacteria,” J. Ram 44(7Spec.), 973–979 (2013).
[Crossref]

Koyama, Y.

Y. Koyama, M. Kuki, P. O. Andersson, and T. Gillbro, “Singlet Excited States and the Light-Harvesting Function of Carotenoids in Bacterial Photosynthesis,” Photochem. Photobiol. 63(3), 243–256 (1996).
[Crossref]

Kuki, M.

Y. Koyama, M. Kuki, P. O. Andersson, and T. Gillbro, “Singlet Excited States and the Light-Harvesting Function of Carotenoids in Bacterial Photosynthesis,” Photochem. Photobiol. 63(3), 243–256 (1996).
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Labroille, G.

Langbein, W.

F. Masia, A. Glen, P. Stephens, P. Borri, and W. Langbein, “Quantitative Chemical Imaging and Unsupervised Analysis Using Hyperspectral Coherent Anti-Stokes Raman Scattering Microscopy,” Anal. Chem. 85(22), 10820–10828 (2013).
[Crossref] [PubMed]

I. Rocha-Mendoza, W. Langbein, and P. Borri, “Coherent anti-Stokes Raman microspectroscopy using spectral focusing with glass dispersion,” Appl. Phys. Lett. 93(20), 201103 (2008).
[Crossref]

Lee, Y. J.

Legouis, R.

Leonardi, P. I.

M. C. Damiani, C. A. Popovich, D. Constenla, and P. I. Leonardi, “Lipid analysis in Haematococcuspluvialis to assess its potential use as a biodiesel feedstock,” Bioresour. Technol. 101(11), 3801–3807 (2010).
[Crossref] [PubMed]

Lin, C.-Y.

Liu, Y.

Lu, Y. F.

Lyn, R. K.

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
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Mahou, P.

Maker, P. D.

P. D. Maker and R. W. Terhune, “Study of Optical Effects Due to an Induced Polarization Third Order in the Electric Field Strength,” Phys. Rev. 137(3A), A801–A818 (1965).
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Masia, F.

F. Masia, A. Glen, P. Stephens, P. Borri, and W. Langbein, “Quantitative Chemical Imaging and Unsupervised Analysis Using Hyperspectral Coherent Anti-Stokes Raman Scattering Microscopy,” Anal. Chem. 85(22), 10820–10828 (2013).
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Matsuura, H.

M. Wayama, S. Ota, H. Matsuura, N. Nango, A. Hirata, and S. Kawano, “Three-Dimensional Ultrastructural Study of Oil and Astaxanthin Accumulation during Encystment in the Green Alga Haematococcus pluvialis,” PLoS ONE 8(1), e53618 (2013).
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McDonald, J. R.

McGinn, P. J.

A. D. Slepkov, A. M. Barlow, A. R. Ridsdale, P. J. McGinn, and A. Stolow, “In vivo hyperspectral CARS and FWM microscopy of carotenoid accumulation in H. Pluvialis,” Proc. SPIE 8937, Multimodal Biomedical Imaging IX, 893709 (2014).

Meyers, S. P.

H.-M. Chen and S. P. Meyers, “A rapid quantitative method for determination of astaxanthin pigment concentration in oil extracts,” J. Am. Oil Chem. Soc. 61(6), 1045–1047 (1984).
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Moffatt, D. J.

A. F. Pegoraro, A. D. Slepkov, A. R. Ridsdale, D. J. Moffatt, and A. Stolow, “Hyperspectral multimodal CARS microscopy in the fingerprint region,” J. Biophotonics 7(1-2), 49–58 (2014).
[Crossref] [PubMed]

A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, and A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
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Müller, M.

Nango, N.

M. Wayama, S. Ota, H. Matsuura, N. Nango, A. Hirata, and S. Kawano, “Three-Dimensional Ultrastructural Study of Oil and Astaxanthin Accumulation during Encystment in the Green Alga Haematococcus pluvialis,” PLoS ONE 8(1), e53618 (2013).
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Nedbal, L.

Z. Pilát, S. Bernatová, J. Ježek, M. Šerý, O. Samek, P. Zemánek, L. Nedbal, and M. Trtílek, “Raman microspectroscopy of algal lipid bodies: β-carotene quantification,” J. Appl. Phycol. 24(3), 541–546 (2012).
[Crossref]

Nibler, J. W.

Nikolaenko, A.

Novotny, L.

J. Renger, R. Quidant, N. v. Hulst, and L. Novotny, “Surface-Enhanced Nonlinear Four-Wave Mixing,” Phys. Rev. Lett. 104, 046803 (2010).

M. Danckwerts and L. Novotny, “Optical Frequency Mixing at Coupled Gold Nanoparticles,” Phys. Rev. Lett. 98(2), 026104 (2007).
[Crossref] [PubMed]

Ogilvie, J. P.

Olaizola, M.

M. Guerin, M. E. Huntley, and M. Olaizola, “Haematococcus astaxanthin: applications for human health and nutrition,” Trends Biotechnol. 21(5), 210–216 (2003).
[Crossref] [PubMed]

Olivier, N.

Ota, S.

M. Wayama, S. Ota, H. Matsuura, N. Nango, A. Hirata, and S. Kawano, “Three-Dimensional Ultrastructural Study of Oil and Astaxanthin Accumulation during Encystment in the Green Alga Haematococcus pluvialis,” PLoS ONE 8(1), e53618 (2013).
[Crossref] [PubMed]

Pegoraro, A. F.

A. F. Pegoraro, A. D. Slepkov, A. R. Ridsdale, D. J. Moffatt, and A. Stolow, “Hyperspectral multimodal CARS microscopy in the fingerprint region,” J. Biophotonics 7(1-2), 49–58 (2014).
[Crossref] [PubMed]

A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, and A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
[Crossref] [PubMed]

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
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Peng, J.

J.-P. Yuan, J. Peng, K. Yin, and J.-H. Wang, “Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae,” Mol. Nutr. Food Res. 55(1), 150–165 (2011).
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Peyriéras, N.

Pezacki, J. P.

A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, and A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
[Crossref] [PubMed]

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
[Crossref] [PubMed]

Pilát, Z.

Z. Pilát, S. Bernatová, J. Ježek, M. Šerý, O. Samek, P. Zemánek, L. Nedbal, and M. Trtílek, “Raman microspectroscopy of algal lipid bodies: β-carotene quantification,” J. Appl. Phycol. 24(3), 541–546 (2012).
[Crossref]

Popovich, C. A.

M. C. Damiani, C. A. Popovich, D. Constenla, and P. I. Leonardi, “Lipid analysis in Haematococcuspluvialis to assess its potential use as a biodiesel feedstock,” Bioresour. Technol. 101(11), 3801–3807 (2010).
[Crossref] [PubMed]

Potma, E. O.

Quidant, R.

J. Renger, R. Quidant, N. v. Hulst, and L. Novotny, “Surface-Enhanced Nonlinear Four-Wave Mixing,” Phys. Rev. Lett. 104, 046803 (2010).

Raghunathan, V.

Renger, J.

J. Renger, R. Quidant, N. v. Hulst, and L. Novotny, “Surface-Enhanced Nonlinear Four-Wave Mixing,” Phys. Rev. Lett. 104, 046803 (2010).

Ridsdale, A.

Ridsdale, A. R.

A. D. Slepkov, A. M. Barlow, A. R. Ridsdale, P. J. McGinn, and A. Stolow, “In vivo hyperspectral CARS and FWM microscopy of carotenoid accumulation in H. Pluvialis,” Proc. SPIE 8937, Multimodal Biomedical Imaging IX, 893709 (2014).

A. F. Pegoraro, A. D. Slepkov, A. R. Ridsdale, D. J. Moffatt, and A. Stolow, “Hyperspectral multimodal CARS microscopy in the fingerprint region,” J. Biophotonics 7(1-2), 49–58 (2014).
[Crossref] [PubMed]

Rimai, L.

L. Rimai, M. E. Heyde, and D. Gill, “Vibrational spectra of some carotenoids and related linear polyenes. Raman spectroscopic study,” J. Am. Chem. Soc. 95(14), 4493–4501 (1973).
[Crossref] [PubMed]

Rinia, H. A.

Rocha-Mendoza, I.

I. Rocha-Mendoza, W. Langbein, and P. Borri, “Coherent anti-Stokes Raman microspectroscopy using spectral focusing with glass dispersion,” Appl. Phys. Lett. 93(20), 201103 (2008).
[Crossref]

Rouleau, Y.

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
[Crossref] [PubMed]

Sagan, S. M.

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
[Crossref] [PubMed]

Samek, O.

Z. Pilát, S. Bernatová, J. Ježek, M. Šerý, O. Samek, P. Zemánek, L. Nedbal, and M. Trtílek, “Raman microspectroscopy of algal lipid bodies: β-carotene quantification,” J. Appl. Phycol. 24(3), 541–546 (2012).
[Crossref]

Šerý, M.

Z. Pilát, S. Bernatová, J. Ježek, M. Šerý, O. Samek, P. Zemánek, L. Nedbal, and M. Trtílek, “Raman microspectroscopy of algal lipid bodies: β-carotene quantification,” J. Appl. Phycol. 24(3), 541–546 (2012).
[Crossref]

Shi, R.

Sintes, J.-M.

Skibsted, L. H.

A. G. Christophersen, H. Jun, K. Jørgensen, and L. H. Skibsted, “Photobleaching of astaxanthin and canthaxanthin,” Z. Lebensm. Unters. Forsch. 192(5), 433–439 (1991).

Slepkov, A. D.

A. F. Pegoraro, A. D. Slepkov, A. R. Ridsdale, D. J. Moffatt, and A. Stolow, “Hyperspectral multimodal CARS microscopy in the fingerprint region,” J. Biophotonics 7(1-2), 49–58 (2014).
[Crossref] [PubMed]

A. D. Slepkov, A. M. Barlow, A. R. Ridsdale, P. J. McGinn, and A. Stolow, “In vivo hyperspectral CARS and FWM microscopy of carotenoid accumulation in H. Pluvialis,” Proc. SPIE 8937, Multimodal Biomedical Imaging IX, 893709 (2014).

Stephens, P.

F. Masia, A. Glen, P. Stephens, P. Borri, and W. Langbein, “Quantitative Chemical Imaging and Unsupervised Analysis Using Hyperspectral Coherent Anti-Stokes Raman Scattering Microscopy,” Anal. Chem. 85(22), 10820–10828 (2013).
[Crossref] [PubMed]

Stolow, A.

A. D. Slepkov, A. M. Barlow, A. R. Ridsdale, P. J. McGinn, and A. Stolow, “In vivo hyperspectral CARS and FWM microscopy of carotenoid accumulation in H. Pluvialis,” Proc. SPIE 8937, Multimodal Biomedical Imaging IX, 893709 (2014).

A. F. Pegoraro, A. D. Slepkov, A. R. Ridsdale, D. J. Moffatt, and A. Stolow, “Hyperspectral multimodal CARS microscopy in the fingerprint region,” J. Biophotonics 7(1-2), 49–58 (2014).
[Crossref] [PubMed]

A. F. Pegoraro, A. Ridsdale, D. J. Moffatt, Y. Jia, J. P. Pezacki, and A. Stolow, “Optimally chirped multimodal CARS microscopy based on a single Ti:sapphire oscillator,” Opt. Express 17(4), 2984–2996 (2009).
[Crossref] [PubMed]

R. K. Lyn, D. C. Kennedy, S. M. Sagan, D. R. Blais, Y. Rouleau, A. F. Pegoraro, X. S. Xie, A. Stolow, and J. P. Pezacki, “Direct imaging of the disruption of hepatitis C virus replication complexes by inhibitors of lipid metabolism,” Virology 394(1), 130–142 (2009).
[Crossref] [PubMed]

Svanberg, U.

C. Brackmann, A. Bengtsson, M. L. Alminger, U. Svanberg, and A. Enejder, “Visualization of beta-carotene and starch granules in plant cells using CARS and SHG microscopy,” J. Ram 42(4Spec.), 586–592 (2011).
[Crossref]

Terhune, R. W.

P. D. Maker and R. W. Terhune, “Study of Optical Effects Due to an Induced Polarization Third Order in the Electric Field Strength,” Phys. Rev. 137(3A), A801–A818 (1965).
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Timlin, J. A.

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J.-P. Yuan, J. Peng, K. Yin, and J.-H. Wang, “Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae,” Mol. Nutr. Food Res. 55(1), 150–165 (2011).
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[PubMed]

Supplementary Material (2)

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Figures (6)

Fig. 1
Fig. 1 Energy level diagrams for four-wave mixing processes with pump at frequency ω1, Stokes at frequency ω2, probe frequency ω3 and anti-Stokes at frequency ω4. (a) Coherent anti-Stokes Raman scattering, vibrationally resonant with a Raman transition of frequency Ω. (b) Non-resonant four-wave mixing. In these experiments, ω1 = ω3.
Fig. 2
Fig. 2 Composite image of various H. pluvialis cells using forward-collected CARS from AXN at 1520 cm−1 (red) and epi-collected TPEF from chlorophyll (green). The cells show several distinctive morphologies, ranging from minimal AXN content within a chlorophyll-dominated cell, to those with several AXN-containing droplets, to cells where AXN almost completely dominates the interior of the cell. Several cells also appear to have large transparent voids within them.
Fig. 3
Fig. 3 3D projection of H. pluvialis cell using forward-collected CARS (red) and epi-directed TPEF (green). (Media 1)
Fig. 4
Fig. 4 (a) Hyperspectral CARS/TPEF image of an algal cell at a Raman shift of 1520 cm−1. (b) Black: Raw CARS spectrum extracted from the highlighted region. Grey: Spontaneous Raman spectrum of AstaREAL standard collected with a Raman spectrometer. Red: The same Raman spectrum after being broadened to the CARS spectral resolution of 30 cm−1.
Fig. 5
Fig. 5 (a) A frame of the motion of a flagellated H. pluvialis cell. The FWM signal is shown in red, the TPEF shown in green. (b) The imaging of an H. pluvialis cyst using FWM. (c) The frequency difference ω1ω2 of the FWM of the highlighted region of (b), shown in green. The frequencies generated by the Stokes supercontinuum (downwards shifted by 7900 cm−1 for overlay purposes) are shown in blue. For comparison, the spontaneous Raman spectrum collected at 785 nm of AstaREAL is plotted in red. (d) The CARS/FWM spectrum of AstaREAL at 860 nm, normalized by the Stokes spectrum. Features below ~1500 cm−1 cannot be resolved due to a lack of Stokes power at these frequencies. (See Media 2)
Fig. 6
Fig. 6 (a) Log-log plot of CARS signal intensity vs. AXN concentration in canola oil, showing a quadratic (slope = 1.94) dependence. (b) (electronic offset baseline-subtracted) CARS spectrum of AXN at 2 mM concentration. (c) CARS (red) / TPEF (green) image of a particular algal cell at a Raman shift of 1520 cm−1. (d) A concentration map of AXN within the cell depicted in (c). The scale bar colour map has units of mM AXN.

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