Abstract

This paper reports the development of a dual-color light sheet fluorescence imaging flow cytometer exclusively designed for rapid phytoplankton analysis. By simultaneously exciting chlorophyll and phycoerythrin fluorescence, the system is enabled to discriminate phycoerythrin-containing and phycoerythrin-lacking phytoplankton groups through simultaneous two-channel spectral imaging-in-flow. It is demonstrated the system has good sensitivity and resolution to detect picophytoplankton down to the size of ~1μm, high throughput of 1.3 × 105cells/s and 5 × 103cells/s at 100μL/min and 3mL/min volume flow rates for cultured picophytoplankton and nanophytoplankton detection, respectively, and a broad imaging range from ~1μm up to 300μm covering most marine phytoplankton cell sizes with just one 40 × objective. The simultaneous realization of high resolution, high sensitivity and high throughput with spectral resolving power of the system is expected to promote the technology towards more practical applications that demand automated phytoplankton analysis.

© 2017 Optical Society of America

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Retraction

This article has been retracted. Please see:
Jianping Li and Zhennan Xu, "Simultaneous dual-color light sheet fluorescence imaging flow cytometry for high-throughput marine phytoplankton analysis: retraction," Opt. Express 25, 20033-20033 (2017)
https://www.osapublishing.org/oe/abstract.cfm?uri=oe-25-17-20033

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References

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2017 (3)

V. Dashkova, D. Malashenkov, N. Poulton, I. Vorobjev, and N. S. Barteneva, “Imaging flow cytometry for phytoplankton analysis,” Methods 112, 188–200 (2017).
[Crossref] [PubMed]

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

E. J. Gualda, H. Pereira, G. G. Martins, R. Gardner, and N. Moreno, “Three-dimensional imaging flow cytometry through light-sheet fluorescence microscopy,” Cytometry A 91(2), 144–151 (2017).
[Crossref] [PubMed]

2016 (4)

P. Paiè, F. Bragheri, A. Bassi, and R. Osellame, “Selective plane illumination microscopy on a chip,” Lab Chip 16(9), 1556–1560 (2016).
[Crossref] [PubMed]

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

C. Lei, T. Ito, M. Ugawa, T. Nozawa, O. Iwata, M. Maki, G. Okada, H. Kobayashi, X. Sun, P. Tiamsak, N. Tsumura, K. Suzuki, D. Di Carlo, Y. Ozeki, and K. Goda, “High-throughput label-free image cytometry and image-based classification of live Euglena gracilis,” Biomed. Opt. Express 7(7), 2703–2708 (2016).
[Crossref] [PubMed]

Q. T. K. Lai, K. C. M. Lee, A. H. L. Tang, K. K. Y. Wong, H. K. H. So, and K. K. Tsia, “High-throughput time-stretch imaging flow cytometry for multi-class classification of phytoplankton,” Opt. Express 24(25), 28170–28184 (2016).
[Crossref] [PubMed]

2015 (1)

E. G. Reynaud, J. Peychl, J. Huisken, and P. Tomancak, “Guide to light-sheet microscopy for adventurous biologists,” Nat. Methods 12(1), 30–34 (2015).
[Crossref] [PubMed]

2014 (3)

C. Yourassowsky and F. Dubois, “High throughput holographic imaging-in-flow for the analysis of a wide plankton size range,” Opt. Express 22(6), 6661–6673 (2014).
[Crossref] [PubMed]

E.-M. Zetsche, A. El Mallahi, F. Dubois, C. Yourassowsky, J. C. Kromkamp, and F. J. R. Meysman, “Imaging-in-Flow: Digital holographic microscopy as a novel tool to detect and classify nanoplanktonic organisms,” Limnol. Oceanogr. Methods 12(11), 757–775 (2014).
[Crossref]

J.-J. Wang and D. L. Tang, “Phytoplankton patchiness during spring intermonsoon in western coast of South China Sea,” Deep Sea Res. Part II Top. Stud. Oceanogr. 101, 120–128 (2014).
[Crossref]

2013 (3)

2012 (2)

T. Govender, L. Ramanna, I. Rawat, and F. Bux, “BODIPY staining, an alternative to the Nile Red fluorescence method for the evaluation of intracellular lipids in microalgae,” Bioresour. Technol. 114, 507–511 (2012).
[Crossref] [PubMed]

J. S. Erickson, N. Hashemi, J. M. Sullivan, A. D. Weidemann, and F. S. Ligler, “In situ phytoplankton analysis: there’s plenty of room at the bottom,” Anal. Chem. 84(2), 839–850 (2012).
[Crossref] [PubMed]

2009 (1)

W. Chen, C. Zhang, L. Song, M. Sommerfeld, and Q. Hu, “A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae,” J. Microbiol. Methods 77(1), 41–47 (2009).
[Crossref] [PubMed]

2007 (3)

M. V. Zubkov, P. H. Burkill, and J. N. Topping, “Flow cytometric enumeration of DNA-stained oceanic planktonic protists,” J. Plankton Res. 29(1), 79–86 (2007).
[Crossref]

W. E. Ortyn, D. J. Perry, V. Venkatachalam, L. Liang, B. E. Hall, K. Frost, and D. A. Basiji, “Extended depth of field imaging for high speed cell analysis,” Cytometry A 71(4), 215–231 (2007).
[Crossref] [PubMed]

R. J. Olson and H. M. Sosik, “A submersible imaging-in-flow instrument to analyze nano-and microplankton: Imaging FlowCytobot,” Limnol. Oceanogr. Methods 5(6), 195–203 (2007).
[Crossref]

2004 (2)

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11, 36–42 (2004).

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

2003 (1)

R. J. Olson, A. Shalapyonok, and H. M. Sosik, “An automated submersible flow cytometer for analyzing pico- and nanophytoplankton: FlowCytobot,” Deep Sea Res. Part I Oceanogr. Res. Pap. 50(2), 301–315 (2003).
[Crossref]

2000 (1)

J. L. Collier, “Flow cytometry and the single cell in phycology,” J. Phycol. 36(4), 628–644 (2000).
[Crossref]

1999 (2)

M. Troussellier, C. Courties, P. Lebaron, and P. Servais, “Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids,” FEMS Microbiol. Ecol. 29(4), 319–330 (1999).
[Crossref]

G. B. Dubelaar, P. L. Gerritzen, A. E. Beeker, R. R. Jonker, and K. Tangen, “Design and first results of CytoBuoy: a wireless flow cytometer for in situ analysis of marine and fresh waters,” Cytometry 37(4), 247–254 (1999).
[Crossref] [PubMed]

1998 (2)

C. K. Sieracki, M. E. Sieracki, and C. S. Yentsch, “An imaging-in-flow system for automated analysis of marine microplankton,” Mar. Ecol. Prog. Ser. 168, 285–296 (1998).
[Crossref]

P. Lebaron, N. Parthuisot, and P. Catala, “Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems,” Appl. Environ. Microbiol. 64(5), 1725–1730 (1998).
[PubMed]

1996 (1)

J. E. Cloern, “Phytoplankton bloom dynamics in coastal ecosystems: a review with some general lessons from sustained investigation of San Francisco Bay, California,” Rev. Geophys. 34(2), 127–168 (1996).
[Crossref]

1989 (3)

D. A. Phinney and T. L. Cucci, “Flow cytometry and phytoplankton,” Cytometry 10(5), 511–521 (1989).
[Crossref] [PubMed]

R. J. Olson, E. R. Zettler, and O. K. Anderson, “Discrimination of eukaryotic phytoplankton cell types from light scatter and autofluorescence properties measured by flow cytometry,” Cytometry 10(5), 636–643 (1989).
[Crossref] [PubMed]

H. Schubert, U. Schiewer, and E. Tschirner, “Fluorescence characteristics of cyanobacteria (blue-green algae),” J. Plankton Res. 11(2), 353–359 (1989).
[Crossref]

1988 (1)

G. T. Evans, “A framework for discussing seasonal succession and coexistence of phytoplankton species,” Limnol. Oceanogr. 33(5), 1027–1036 (1988).
[Crossref]

Abbriano, R.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Abràmoff, M. D.

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11, 36–42 (2004).

Alderete, B.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Anderson, O. K.

R. J. Olson, E. R. Zettler, and O. K. Anderson, “Discrimination of eukaryotic phytoplankton cell types from light scatter and autofluorescence properties measured by flow cytometry,” Cytometry 10(5), 636–643 (1989).
[Crossref] [PubMed]

Barteneva, N. S.

V. Dashkova, D. Malashenkov, N. Poulton, I. Vorobjev, and N. S. Barteneva, “Imaging flow cytometry for phytoplankton analysis,” Methods 112, 188–200 (2017).
[Crossref] [PubMed]

Basiji, D. A.

W. E. Ortyn, D. J. Perry, V. Venkatachalam, L. Liang, B. E. Hall, K. Frost, and D. A. Basiji, “Extended depth of field imaging for high speed cell analysis,” Cytometry A 71(4), 215–231 (2007).
[Crossref] [PubMed]

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Bassi, A.

P. Paiè, F. Bragheri, A. Bassi, and R. Osellame, “Selective plane illumination microscopy on a chip,” Lab Chip 16(9), 1556–1560 (2016).
[Crossref] [PubMed]

Beeker, A. E.

G. B. Dubelaar, P. L. Gerritzen, A. E. Beeker, R. R. Jonker, and K. Tangen, “Design and first results of CytoBuoy: a wireless flow cytometer for in situ analysis of marine and fresh waters,” Cytometry 37(4), 247–254 (1999).
[Crossref] [PubMed]

Bragheri, F.

P. Paiè, F. Bragheri, A. Bassi, and R. Osellame, “Selective plane illumination microscopy on a chip,” Lab Chip 16(9), 1556–1560 (2016).
[Crossref] [PubMed]

Buchholz, J.

Burkill, P. H.

M. V. Zubkov, P. H. Burkill, and J. N. Topping, “Flow cytometric enumeration of DNA-stained oceanic planktonic protists,” J. Plankton Res. 29(1), 79–86 (2007).
[Crossref]

Bux, F.

T. Govender, L. Ramanna, I. Rawat, and F. Bux, “BODIPY staining, an alternative to the Nile Red fluorescence method for the evaluation of intracellular lipids in microalgae,” Bioresour. Technol. 114, 507–511 (2012).
[Crossref] [PubMed]

Catala, P.

P. Lebaron, N. Parthuisot, and P. Catala, “Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems,” Appl. Environ. Microbiol. 64(5), 1725–1730 (1998).
[PubMed]

Chan, R. K. Y.

Charbon, E.

Chen, W.

W. Chen, C. Zhang, L. Song, M. Sommerfeld, and Q. Hu, “A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae,” J. Microbiol. Methods 77(1), 41–47 (2009).
[Crossref] [PubMed]

Cloern, J. E.

J. E. Cloern, “Phytoplankton bloom dynamics in coastal ecosystems: a review with some general lessons from sustained investigation of San Francisco Bay, California,” Rev. Geophys. 34(2), 127–168 (1996).
[Crossref]

Collier, J. L.

J. L. Collier, “Flow cytometry and the single cell in phycology,” J. Phycol. 36(4), 628–644 (2000).
[Crossref]

Cook, O.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Courties, C.

M. Troussellier, C. Courties, P. Lebaron, and P. Servais, “Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids,” FEMS Microbiol. Ecol. 29(4), 319–330 (1999).
[Crossref]

Cucci, T. L.

D. A. Phinney and T. L. Cucci, “Flow cytometry and phytoplankton,” Cytometry 10(5), 511–521 (1989).
[Crossref] [PubMed]

Dashkova, V.

V. Dashkova, D. Malashenkov, N. Poulton, I. Vorobjev, and N. S. Barteneva, “Imaging flow cytometry for phytoplankton analysis,” Methods 112, 188–200 (2017).
[Crossref] [PubMed]

Davis, A.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Di Carlo, D.

Donati, L.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Dubelaar, G. B.

G. B. Dubelaar, P. L. Gerritzen, A. E. Beeker, R. R. Jonker, and K. Tangen, “Design and first results of CytoBuoy: a wireless flow cytometer for in situ analysis of marine and fresh waters,” Cytometry 37(4), 247–254 (1999).
[Crossref] [PubMed]

Dubois, F.

C. Yourassowsky and F. Dubois, “High throughput holographic imaging-in-flow for the analysis of a wide plankton size range,” Opt. Express 22(6), 6661–6673 (2014).
[Crossref] [PubMed]

E.-M. Zetsche, A. El Mallahi, F. Dubois, C. Yourassowsky, J. C. Kromkamp, and F. J. R. Meysman, “Imaging-in-Flow: Digital holographic microscopy as a novel tool to detect and classify nanoplanktonic organisms,” Limnol. Oceanogr. Methods 12(11), 757–775 (2014).
[Crossref]

El Mallahi, A.

E.-M. Zetsche, A. El Mallahi, F. Dubois, C. Yourassowsky, J. C. Kromkamp, and F. J. R. Meysman, “Imaging-in-Flow: Digital holographic microscopy as a novel tool to detect and classify nanoplanktonic organisms,” Limnol. Oceanogr. Methods 12(11), 757–775 (2014).
[Crossref]

Erickson, J. S.

J. S. Erickson, N. Hashemi, J. M. Sullivan, A. D. Weidemann, and F. S. Ligler, “In situ phytoplankton analysis: there’s plenty of room at the bottom,” Anal. Chem. 84(2), 839–850 (2012).
[Crossref] [PubMed]

Evans, G. T.

G. T. Evans, “A framework for discussing seasonal succession and coexistence of phytoplankton species,” Limnol. Oceanogr. 33(5), 1027–1036 (1988).
[Crossref]

Fortun, D.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Frost, K.

W. E. Ortyn, D. J. Perry, V. Venkatachalam, L. Liang, B. E. Hall, K. Frost, and D. A. Basiji, “Extended depth of field imaging for high speed cell analysis,” Cytometry A 71(4), 215–231 (2007).
[Crossref] [PubMed]

Gardner, R.

E. J. Gualda, H. Pereira, G. G. Martins, R. Gardner, and N. Moreno, “Three-dimensional imaging flow cytometry through light-sheet fluorescence microscopy,” Cytometry A 91(2), 144–151 (2017).
[Crossref] [PubMed]

George, T. C.

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Gerritzen, P. L.

G. B. Dubelaar, P. L. Gerritzen, A. E. Beeker, R. R. Jonker, and K. Tangen, “Design and first results of CytoBuoy: a wireless flow cytometer for in situ analysis of marine and fresh waters,” Cytometry 37(4), 247–254 (1999).
[Crossref] [PubMed]

Goda, K.

Govender, T.

T. Govender, L. Ramanna, I. Rawat, and F. Bux, “BODIPY staining, an alternative to the Nile Red fluorescence method for the evaluation of intracellular lipids in microalgae,” Bioresour. Technol. 114, 507–511 (2012).
[Crossref] [PubMed]

Gualda, E. J.

E. J. Gualda, H. Pereira, G. G. Martins, R. Gardner, and N. Moreno, “Three-dimensional imaging flow cytometry through light-sheet fluorescence microscopy,” Cytometry A 91(2), 144–151 (2017).
[Crossref] [PubMed]

Guiet, R.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Hall, B. E.

W. E. Ortyn, D. J. Perry, V. Venkatachalam, L. Liang, B. E. Hall, K. Frost, and D. A. Basiji, “Extended depth of field imaging for high speed cell analysis,” Cytometry A 71(4), 215–231 (2007).
[Crossref] [PubMed]

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Hashemi, N.

J. S. Erickson, N. Hashemi, J. M. Sullivan, A. D. Weidemann, and F. S. Ligler, “In situ phytoplankton analysis: there’s plenty of room at the bottom,” Anal. Chem. 84(2), 839–850 (2012).
[Crossref] [PubMed]

Hildebrand, M.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Hu, Q.

W. Chen, C. Zhang, L. Song, M. Sommerfeld, and Q. Hu, “A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae,” J. Microbiol. Methods 77(1), 41–47 (2009).
[Crossref] [PubMed]

Huisken, J.

E. G. Reynaud, J. Peychl, J. Huisken, and P. Tomancak, “Guide to light-sheet microscopy for adventurous biologists,” Nat. Methods 12(1), 30–34 (2015).
[Crossref] [PubMed]

Ito, T.

Iwata, O.

Jonker, R. R.

G. B. Dubelaar, P. L. Gerritzen, A. E. Beeker, R. R. Jonker, and K. Tangen, “Design and first results of CytoBuoy: a wireless flow cytometer for in situ analysis of marine and fresh waters,” Cytometry 37(4), 247–254 (1999).
[Crossref] [PubMed]

Kobayashi, H.

Krieger, J. W.

Kromkamp, J. C.

E.-M. Zetsche, A. El Mallahi, F. Dubois, C. Yourassowsky, J. C. Kromkamp, and F. J. R. Meysman, “Imaging-in-Flow: Digital holographic microscopy as a novel tool to detect and classify nanoplanktonic organisms,” Limnol. Oceanogr. Methods 12(11), 757–775 (2014).
[Crossref]

Lai, Q. T. K.

Langowski, J.

Lebaron, P.

M. Troussellier, C. Courties, P. Lebaron, and P. Servais, “Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids,” FEMS Microbiol. Ecol. 29(4), 319–330 (1999).
[Crossref]

P. Lebaron, N. Parthuisot, and P. Catala, “Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems,” Appl. Environ. Microbiol. 64(5), 1725–1730 (1998).
[PubMed]

Lee, K. C. M.

Lei, C.

Li, J.

Liang, L.

W. E. Ortyn, D. J. Perry, V. Venkatachalam, L. Liang, B. E. Hall, K. Frost, and D. A. Basiji, “Extended depth of field imaging for high speed cell analysis,” Cytometry A 71(4), 215–231 (2007).
[Crossref] [PubMed]

Ligler, F. S.

J. S. Erickson, N. Hashemi, J. M. Sullivan, A. D. Weidemann, and F. S. Ligler, “In situ phytoplankton analysis: there’s plenty of room at the bottom,” Anal. Chem. 84(2), 839–850 (2012).
[Crossref] [PubMed]

Lynch, D. H.

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Magalhães, P. J.

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11, 36–42 (2004).

Maki, M.

Malashenkov, D.

V. Dashkova, D. Malashenkov, N. Poulton, I. Vorobjev, and N. S. Barteneva, “Imaging flow cytometry for phytoplankton analysis,” Methods 112, 188–200 (2017).
[Crossref] [PubMed]

Manandhar-Shrestha, K.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Martins, G. G.

E. J. Gualda, H. Pereira, G. G. Martins, R. Gardner, and N. Moreno, “Three-dimensional imaging flow cytometry through light-sheet fluorescence microscopy,” Cytometry A 91(2), 144–151 (2017).
[Crossref] [PubMed]

Meysman, F. J. R.

E.-M. Zetsche, A. El Mallahi, F. Dubois, C. Yourassowsky, J. C. Kromkamp, and F. J. R. Meysman, “Imaging-in-Flow: Digital holographic microscopy as a novel tool to detect and classify nanoplanktonic organisms,” Limnol. Oceanogr. Methods 12(11), 757–775 (2014).
[Crossref]

Moreno, N.

E. J. Gualda, H. Pereira, G. G. Martins, R. Gardner, and N. Moreno, “Three-dimensional imaging flow cytometry through light-sheet fluorescence microscopy,” Cytometry A 91(2), 144–151 (2017).
[Crossref] [PubMed]

Morrissey, P. J.

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Nozawa, T.

Okada, G.

Olson, R. J.

R. J. Olson and H. M. Sosik, “A submersible imaging-in-flow instrument to analyze nano-and microplankton: Imaging FlowCytobot,” Limnol. Oceanogr. Methods 5(6), 195–203 (2007).
[Crossref]

R. J. Olson, A. Shalapyonok, and H. M. Sosik, “An automated submersible flow cytometer for analyzing pico- and nanophytoplankton: FlowCytobot,” Deep Sea Res. Part I Oceanogr. Res. Pap. 50(2), 301–315 (2003).
[Crossref]

R. J. Olson, E. R. Zettler, and O. K. Anderson, “Discrimination of eukaryotic phytoplankton cell types from light scatter and autofluorescence properties measured by flow cytometry,” Cytometry 10(5), 636–643 (1989).
[Crossref] [PubMed]

Ortyn, W. E.

W. E. Ortyn, D. J. Perry, V. Venkatachalam, L. Liang, B. E. Hall, K. Frost, and D. A. Basiji, “Extended depth of field imaging for high speed cell analysis,” Cytometry A 71(4), 215–231 (2007).
[Crossref] [PubMed]

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Osellame, R.

P. Paiè, F. Bragheri, A. Bassi, and R. Osellame, “Selective plane illumination microscopy on a chip,” Lab Chip 16(9), 1556–1560 (2016).
[Crossref] [PubMed]

Ozeki, Y.

Paiè, P.

P. Paiè, F. Bragheri, A. Bassi, and R. Osellame, “Selective plane illumination microscopy on a chip,” Lab Chip 16(9), 1556–1560 (2016).
[Crossref] [PubMed]

Parthuisot, N.

P. Lebaron, N. Parthuisot, and P. Catala, “Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems,” Appl. Environ. Microbiol. 64(5), 1725–1730 (1998).
[PubMed]

Pereira, H.

E. J. Gualda, H. Pereira, G. G. Martins, R. Gardner, and N. Moreno, “Three-dimensional imaging flow cytometry through light-sheet fluorescence microscopy,” Cytometry A 91(2), 144–151 (2017).
[Crossref] [PubMed]

Perry, D. J.

W. E. Ortyn, D. J. Perry, V. Venkatachalam, L. Liang, B. E. Hall, K. Frost, and D. A. Basiji, “Extended depth of field imaging for high speed cell analysis,” Cytometry A 71(4), 215–231 (2007).
[Crossref] [PubMed]

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Peychl, J.

E. G. Reynaud, J. Peychl, J. Huisken, and P. Tomancak, “Guide to light-sheet microscopy for adventurous biologists,” Nat. Methods 12(1), 30–34 (2015).
[Crossref] [PubMed]

Phinney, D. A.

D. A. Phinney and T. L. Cucci, “Flow cytometry and phytoplankton,” Cytometry 10(5), 511–521 (1989).
[Crossref] [PubMed]

Poulton, N.

V. Dashkova, D. Malashenkov, N. Poulton, I. Vorobjev, and N. S. Barteneva, “Imaging flow cytometry for phytoplankton analysis,” Methods 112, 188–200 (2017).
[Crossref] [PubMed]

Pugsley, H. R.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Ram, S. J.

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11, 36–42 (2004).

Ramanna, L.

T. Govender, L. Ramanna, I. Rawat, and F. Bux, “BODIPY staining, an alternative to the Nile Red fluorescence method for the evaluation of intracellular lipids in microalgae,” Bioresour. Technol. 114, 507–511 (2012).
[Crossref] [PubMed]

Rawat, I.

T. Govender, L. Ramanna, I. Rawat, and F. Bux, “BODIPY staining, an alternative to the Nile Red fluorescence method for the evaluation of intracellular lipids in microalgae,” Bioresour. Technol. 114, 507–511 (2012).
[Crossref] [PubMed]

Reynaud, E. G.

E. G. Reynaud, J. Peychl, J. Huisken, and P. Tomancak, “Guide to light-sheet microscopy for adventurous biologists,” Nat. Methods 12(1), 30–34 (2015).
[Crossref] [PubMed]

Sage, D.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Sánchez-Alvarez, E. L.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Schiewer, U.

H. Schubert, U. Schiewer, and E. Tschirner, “Fluorescence characteristics of cyanobacteria (blue-green algae),” J. Plankton Res. 11(2), 353–359 (1989).
[Crossref]

Schmit, G.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Schubert, H.

H. Schubert, U. Schiewer, and E. Tschirner, “Fluorescence characteristics of cyanobacteria (blue-green algae),” J. Plankton Res. 11(2), 353–359 (1989).
[Crossref]

Seitz, A.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Seo, M. J.

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Servais, P.

M. Troussellier, C. Courties, P. Lebaron, and P. Servais, “Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids,” FEMS Microbiol. Ecol. 29(4), 319–330 (1999).
[Crossref]

Shalapyonok, A.

R. J. Olson, A. Shalapyonok, and H. M. Sosik, “An automated submersible flow cytometer for analyzing pico- and nanophytoplankton: FlowCytobot,” Deep Sea Res. Part I Oceanogr. Res. Pap. 50(2), 301–315 (2003).
[Crossref]

Shrestha, R. P.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Sieracki, C. K.

C. K. Sieracki, M. E. Sieracki, and C. S. Yentsch, “An imaging-in-flow system for automated analysis of marine microplankton,” Mar. Ecol. Prog. Ser. 168, 285–296 (1998).
[Crossref]

Sieracki, M. E.

C. K. Sieracki, M. E. Sieracki, and C. S. Yentsch, “An imaging-in-flow system for automated analysis of marine microplankton,” Mar. Ecol. Prog. Ser. 168, 285–296 (1998).
[Crossref]

Singh, A. P.

Smith, S. R.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

So, H. K. H.

Sommerfeld, M.

W. Chen, C. Zhang, L. Song, M. Sommerfeld, and Q. Hu, “A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae,” J. Microbiol. Methods 77(1), 41–47 (2009).
[Crossref] [PubMed]

Song, L.

W. Chen, C. Zhang, L. Song, M. Sommerfeld, and Q. Hu, “A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae,” J. Microbiol. Methods 77(1), 41–47 (2009).
[Crossref] [PubMed]

Sosik, H. M.

R. J. Olson and H. M. Sosik, “A submersible imaging-in-flow instrument to analyze nano-and microplankton: Imaging FlowCytobot,” Limnol. Oceanogr. Methods 5(6), 195–203 (2007).
[Crossref]

R. J. Olson, A. Shalapyonok, and H. M. Sosik, “An automated submersible flow cytometer for analyzing pico- and nanophytoplankton: FlowCytobot,” Deep Sea Res. Part I Oceanogr. Res. Pap. 50(2), 301–315 (2003).
[Crossref]

Soulez, F.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Sullivan, J. M.

J. S. Erickson, N. Hashemi, J. M. Sullivan, A. D. Weidemann, and F. S. Ligler, “In situ phytoplankton analysis: there’s plenty of room at the bottom,” Anal. Chem. 84(2), 839–850 (2012).
[Crossref] [PubMed]

Sun, X.

Suzuki, K.

Tang, A. H. L.

Tang, D. L.

J.-J. Wang and D. L. Tang, “Phytoplankton patchiness during spring intermonsoon in western coast of South China Sea,” Deep Sea Res. Part II Top. Stud. Oceanogr. 101, 120–128 (2014).
[Crossref]

Tangen, K.

G. B. Dubelaar, P. L. Gerritzen, A. E. Beeker, R. R. Jonker, and K. Tangen, “Design and first results of CytoBuoy: a wireless flow cytometer for in situ analysis of marine and fresh waters,” Cytometry 37(4), 247–254 (1999).
[Crossref] [PubMed]

Tiamsak, P.

Tomancak, P.

E. G. Reynaud, J. Peychl, J. Huisken, and P. Tomancak, “Guide to light-sheet microscopy for adventurous biologists,” Nat. Methods 12(1), 30–34 (2015).
[Crossref] [PubMed]

Topping, J. N.

M. V. Zubkov, P. H. Burkill, and J. N. Topping, “Flow cytometric enumeration of DNA-stained oceanic planktonic protists,” J. Plankton Res. 29(1), 79–86 (2007).
[Crossref]

Traller, J. C.

M. Hildebrand, A. Davis, R. Abbriano, H. R. Pugsley, J. C. Traller, S. R. Smith, R. P. Shrestha, O. Cook, E. L. Sánchez-Alvarez, K. Manandhar-Shrestha, and B. Alderete, “Applications of imaging flow cytometry for microalgae,” Methods Mol. Biol. 1389, 47–67 (2016).
[Crossref] [PubMed]

Troussellier, M.

M. Troussellier, C. Courties, P. Lebaron, and P. Servais, “Flow cytometric discrimination of bacterial populations in seawater based on SYTO 13 staining of nucleic acids,” FEMS Microbiol. Ecol. 29(4), 319–330 (1999).
[Crossref]

Tschirner, E.

H. Schubert, U. Schiewer, and E. Tschirner, “Fluorescence characteristics of cyanobacteria (blue-green algae),” J. Plankton Res. 11(2), 353–359 (1989).
[Crossref]

Tsia, K. K.

Tsumura, N.

Ugawa, M.

Unser, M.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Venkatachalam, V.

W. E. Ortyn, D. J. Perry, V. Venkatachalam, L. Liang, B. E. Hall, K. Frost, and D. A. Basiji, “Extended depth of field imaging for high speed cell analysis,” Cytometry A 71(4), 215–231 (2007).
[Crossref] [PubMed]

Vonesch, C.

D. Sage, L. Donati, F. Soulez, D. Fortun, G. Schmit, A. Seitz, R. Guiet, C. Vonesch, and M. Unser, “DeconvolutionLab2: An Open-Source Software for Deconvolution Microscopy,” Methods 115, 28–41 (2017).
[Crossref] [PubMed]

Vorobjev, I.

V. Dashkova, D. Malashenkov, N. Poulton, I. Vorobjev, and N. S. Barteneva, “Imaging flow cytometry for phytoplankton analysis,” Methods 112, 188–200 (2017).
[Crossref] [PubMed]

Wang, J.-J.

J.-J. Wang and D. L. Tang, “Phytoplankton patchiness during spring intermonsoon in western coast of South China Sea,” Deep Sea Res. Part II Top. Stud. Oceanogr. 101, 120–128 (2014).
[Crossref]

Weidemann, A. D.

J. S. Erickson, N. Hashemi, J. M. Sullivan, A. D. Weidemann, and F. S. Ligler, “In situ phytoplankton analysis: there’s plenty of room at the bottom,” Anal. Chem. 84(2), 839–850 (2012).
[Crossref] [PubMed]

Wohland, T.

Wong, K. K. Y.

Wu, J.

Yentsch, C. S.

C. K. Sieracki, M. E. Sieracki, and C. S. Yentsch, “An imaging-in-flow system for automated analysis of marine microplankton,” Mar. Ecol. Prog. Ser. 168, 285–296 (1998).
[Crossref]

Yourassowsky, C.

C. Yourassowsky and F. Dubois, “High throughput holographic imaging-in-flow for the analysis of a wide plankton size range,” Opt. Express 22(6), 6661–6673 (2014).
[Crossref] [PubMed]

E.-M. Zetsche, A. El Mallahi, F. Dubois, C. Yourassowsky, J. C. Kromkamp, and F. J. R. Meysman, “Imaging-in-Flow: Digital holographic microscopy as a novel tool to detect and classify nanoplanktonic organisms,” Limnol. Oceanogr. Methods 12(11), 757–775 (2014).
[Crossref]

Zetsche, E.-M.

E.-M. Zetsche, A. El Mallahi, F. Dubois, C. Yourassowsky, J. C. Kromkamp, and F. J. R. Meysman, “Imaging-in-Flow: Digital holographic microscopy as a novel tool to detect and classify nanoplanktonic organisms,” Limnol. Oceanogr. Methods 12(11), 757–775 (2014).
[Crossref]

Zettler, E. R.

R. J. Olson, E. R. Zettler, and O. K. Anderson, “Discrimination of eukaryotic phytoplankton cell types from light scatter and autofluorescence properties measured by flow cytometry,” Cytometry 10(5), 636–643 (1989).
[Crossref] [PubMed]

Zhang, C.

W. Chen, C. Zhang, L. Song, M. Sommerfeld, and Q. Hu, “A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae,” J. Microbiol. Methods 77(1), 41–47 (2009).
[Crossref] [PubMed]

Zimmerman, C. A.

T. C. George, D. A. Basiji, B. E. Hall, D. H. Lynch, W. E. Ortyn, D. J. Perry, M. J. Seo, C. A. Zimmerman, and P. J. Morrissey, “Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer,” Cytometry A 59(2), 237–245 (2004).
[Crossref] [PubMed]

Zubkov, M. V.

M. V. Zubkov, P. H. Burkill, and J. N. Topping, “Flow cytometric enumeration of DNA-stained oceanic planktonic protists,” J. Plankton Res. 29(1), 79–86 (2007).
[Crossref]

Anal. Chem. (1)

J. S. Erickson, N. Hashemi, J. M. Sullivan, A. D. Weidemann, and F. S. Ligler, “In situ phytoplankton analysis: there’s plenty of room at the bottom,” Anal. Chem. 84(2), 839–850 (2012).
[Crossref] [PubMed]

Appl. Environ. Microbiol. (1)

P. Lebaron, N. Parthuisot, and P. Catala, “Comparison of blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems,” Appl. Environ. Microbiol. 64(5), 1725–1730 (1998).
[PubMed]

Biomed. Opt. Express (1)

Biophoton. Int. (1)

M. D. Abràmoff, P. J. Magalhães, and S. J. Ram, “Image processing with ImageJ,” Biophoton. Int. 11, 36–42 (2004).

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Figures (7)

Fig. 1
Fig. 1 Schematic of the DC-LSF-IFC system. M1-M5: dielectric flat mirrors; L1-L2: lenses; IR: iris; CL: cylindrical lens; EO: excitation objective lens; DO: detection objective lens; LP: long-pass filter; DC1-DC3: long-pass dichroic filters; BP1-BP2: band-pass filters; ND1-ND2: neutral density filters; TL: tube lens; DL: demagnifying lens.
Fig. 2
Fig. 2 Schematics of LSF-IFC image formation. (a) Imaging fluorescent particles larger than laser-sheet thickness; (b) Imaging fluorescent particles smaller than laser-sheet thickness.
Fig. 3
Fig. 3 (a) Light sheet cross-section images at various X positions, bar = 100μm; (b) Light sheets thickness variation at different X positions; (c) and (d) Lateral PSFs of the orange and red imaging channels, respectively.
Fig. 4
Fig. 4 (a) and (b) Bright-field and epifluorescence microscopy images of Synechococcus CCMA299, bar = 50μm; (c) and (d) Red- and orange-channel DC-LSF-IFC images of Synechococcus CCMA299; (e) and (f) Red- and orange-channel DC-LSF-IFC images of Synechococcus CCMA300; (g) and (h) Red- and orange-channel DC-LSF-IFC images of Prochlorococcus sp. (i) Bright-field microcopy images of Chlorella sp. (top row) and Porphyridium sp. (bottom row), bar = 5μm; (j) and (k) Red- and orange-channel DC-LSF-IFC images of Chlorella sp. and Porphyridium sp. mixed sample; (l) Pseudo-color composite image of (j) and (k). For DC-LSF-IFC captured images, frame size = 300μm × 300μm, and red frames correspond to Chl a-channel and orange frames correspond to PE-channel, respectively.
Fig. 5
Fig. 5 Cell quantitation results of (a) Synechococcus CCMA299 and (b) mixture of Porphyridium sp. and Chlorella sp. by DC-LSF-IFC analysis.
Fig. 6
Fig. 6 Selected collection of raw images of natural coastal seawater sample acquired by the DC-LSF-IFC system. Frame size = 300μm × 300μm, and red frames correspond to Chl a-channel and orange frames correspond to PE-channel, respectively.
Fig. 7
Fig. 7 Selected large phytoplankton cell images captured by the DC-LSF-IFC system from natural coastal seawater samples. Frame size = 300μm × 300μm and red frames correspond to Chl a-channel.

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