Abstract

Microalga-based biomaterial production has attracted attention as a new source of drugs, foods, and biofuels. For enhancing the production efficiency, it is essential to understand its differences between heterogeneous microalgal subpopulations. However, existing techniques are not adequate to address the need due to the lack of single-cell resolution or the inability to perform large-scale analysis and detect small molecules. Here we demonstrated large-scale single-cell analysis of Euglena gracilis (a unicellular microalgal species that produces paramylon as a potential drug for HIV and colon cancer) with our recently developed high-throughput broadband Raman flow cytometer at a throughput of >1,000 cells/s. Specifically, we characterized the intracellular content of paramylon from single-cell Raman spectra of 10,000 E. gracilis cells cultured under five different conditions and found that paramylon contents in E. gracilis cells cultured in an identical condition is given by a log-normal distribution, which is a good model for describing the number of chemicals in a reaction network. The capability of characterizing distribution functions in a label-free manner is an important basis for isolating specific cell populations for synthetic biology via directed evolution based on the intracellular content of metabolites.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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  2. S. Kottuparambil, R. L. Thankamony, and S. Agusti, “Euglena as a potential natural source of value-added metabolites. A review,” Algal Res. 37, 154–159 (2019).
    [Crossref]
  3. A. Joseph, S. Aikawa, K. Sasaki, F. Matsuda, T. Hasunuma, and A. Kondo, “Increased biomass production and glycogen accumulation in apcE gene deleted Synechocystis sp. PCC 6803,” AMB Express 4(1), 17 (2014).
    [Crossref]
  4. G. K. Kumaraswamy, T. Guerra, X. Qian, S. Zhang, D. A. Bryant, and G. C. Dismukes, “Reprogramming the glycolytic pathway for increased hydrogen production in cyanobacteria: metabolic engineering of NAD+-dependent GAPDH,” Energy Environ. Sci. 6(12), 3722–3731 (2013).
    [Crossref]
  5. T.-J. Chow, H.-Y. Su, T.-Y. Tsai, H.-H. Chou, T.-M. Lee, and J.-S. Chang, “Using recombinant cyanobacterium (Synechococcus elongatus) with increased carbohydrate productivity as feedstock for bioethanol production via separate hydrolysis and fermentation process,” Bioresour. Technol. 184, 33–41 (2015).
    [Crossref]
  6. S. Aikawa, S.-H. Ho, A. Nakanishi, J.-S. Chang, T. Hasunuma, and A. Kondo, “Improving polyglucan production in cyanobacteria and microalgae via cultivation design and metabolic engineering,” Biotechnol. J. 10(6), 886–898 (2015).
    [Crossref]
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  17. P. Zhang, L. Ren, X. Zhang, Y. Shan, Y. Wang, Y. Ji, H. Yin, W. E. Huang, J. Xu, and B. Ma, “Raman-Activated Cell Sorting Based on Dielectrophoretic Single-Cell Trap and Release,” Anal. Chem. 87(4), 2282–2289 (2015).
    [Crossref]
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    [Crossref]
  19. K. Hiramatsu, T. Ideguchi, Y. Yonamine, S. Lee, Y. Luo, K. Hashimoto, T. Ito, M. Hase, J.-W. Park, Y. Kasai, S. Sakuma, T. Hayakawa, F. Arai, Y. Hoshino, and K. Goda, “High-throughput label-free molecular fingerprinting flow cytometry,” Sci. Adv. 5(1), eaau0241 (2019).
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    [Crossref]
  21. S. C. Feldman, S. Reynaldi, C. A. Stortz, A. S. Cerezo, and E. B. Damonte, “Antiviral properties of fucoidan fractions from Leathesia difformis,” Phytomedicine 6(5), 335–340 (1999).
    [Crossref]
  22. T. Watanabe, R. Shimada, A. Matsuyama, M. Yuasa, H. Sawamura, E. Yoshida, and K. Suzuki, “Antitumor activity of the β-glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice,” Food Funct. 4(11), 1685–1690 (2013).
    [Crossref]
  23. A. Demirbas and M. Fatih Demirbas, “Importance of algae oil as a source of biodiesel,” Energy Convers. Manage. 52(1), 163–170 (2011).
    [Crossref]
  24. C. Furusawa, T. Suzuki, A. Kashiwagi, T. Yomo, and K. Kaneko, “Ubiquity of log-normal distributions in intra-cellular reaction dynamics,” Biophysics (Biophys. Soc. Jpn.) 1, 25–31 (2005).
    [Crossref]
  25. E. Limpert, W. A. Stahel, and M. Abbt, “Log-normal Distributions across the Sciences: Keys and Clues,” BioScience 51(5), 341–352 (2001).
    [Crossref]
  26. Y. Oda, Y. Nakano, and S. Kitaoka, “Utilization and Toxicity of Exogenous Amino Acids in Euglena gracilis,” Microbiology (London, U. K.) 128(4), 853–858 (1982).
    [Crossref]
  27. L. E. Koren and S. H. Hutner, “High-yield media for photosynthesizing Euglena gracilis Z,” J. Protozool. 14, 17 (1967).
  28. L. Barsanti, R. Vismara, V. Passarelli, and P. Gualtieri, “Paramylon (β-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis. Effects of growth conditions,” J. Appl. Phycol. 13(1), 59–65 (2001).
    [Crossref]
  29. K. Yamada, H. Suzuki, T. Takeuchi, Y. Kazama, S. Mitra, T. Abe, K. Goda, K. Suzuki, and O. Iwata, “Efficient selective breeding of live oil-rich Euglena gracilis with fluorescence-activated cell sorting,” Sci. Rep. 6(1), 26327 (2016).
    [Crossref]

2019 (3)

S. Kottuparambil, R. L. Thankamony, and S. Agusti, “Euglena as a potential natural source of value-added metabolites. A review,” Algal Res. 37, 154–159 (2019).
[Crossref]

A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
[Crossref]

K. Hiramatsu, T. Ideguchi, Y. Yonamine, S. Lee, Y. Luo, K. Hashimoto, T. Ito, M. Hase, J.-W. Park, Y. Kasai, S. Sakuma, T. Hayakawa, F. Arai, Y. Hoshino, and K. Goda, “High-throughput label-free molecular fingerprinting flow cytometry,” Sci. Adv. 5(1), eaau0241 (2019).
[Crossref]

2018 (2)

X. Jing, H. Gou, Y. Gong, X. Su, L. Xu, Y. Ji, Y. Song, I. P. Thompson, J. Xu, and W. E. Huang, “Raman-activated cell sorting and metagenomic sequencing revealing carbon-fixing bacteria in the ocean,” Environ. Microbiol. 20(6), 2241–2255 (2018).
[Crossref]

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
[Crossref]

2017 (1)

A. K. Bajhaiya, J. Ziehe Moreira, and J. K. Pittman, “Transcriptional Engineering of Microalgae: Prospects for High-Value Chemicals,” Trends Biotechnol. 35(2), 95–99 (2017).
[Crossref]

2016 (4)

Y. Song, H. Yin, and W. E. Huang, “Raman activated cell sorting,” Curr. Opin. Chem. Biol. 33, 1–8 (2016).
[Crossref]

N. Wang, B. Guan, Q. Kong, H. Sun, Z. Geng, and L. Duan, “Enhancement of astaxanthin production from Haematococcus pluvialis mutants by three-stage mutagenesis breeding,” J. Biotechnol. 236, 71–77 (2016).
[Crossref]

Y. Wakisaka, Y. Suzuki, O. Iwata, A. Nakashima, T. Ito, M. Hirose, R. Domon, M. Sugawara, N. Tsumura, H. Watarai, T. Shimobaba, K. Suzuki, K. Goda, and Y. Ozeki, “Probing the metabolic heterogeneity of live Euglena gracilis with stimulated Raman scattering microscopy,” Nat. Microbiol. 1(10), 16124 (2016).
[Crossref]

K. Yamada, H. Suzuki, T. Takeuchi, Y. Kazama, S. Mitra, T. Abe, K. Goda, K. Suzuki, and O. Iwata, “Efficient selective breeding of live oil-rich Euglena gracilis with fluorescence-activated cell sorting,” Sci. Rep. 6(1), 26327 (2016).
[Crossref]

2015 (3)

T.-J. Chow, H.-Y. Su, T.-Y. Tsai, H.-H. Chou, T.-M. Lee, and J.-S. Chang, “Using recombinant cyanobacterium (Synechococcus elongatus) with increased carbohydrate productivity as feedstock for bioethanol production via separate hydrolysis and fermentation process,” Bioresour. Technol. 184, 33–41 (2015).
[Crossref]

S. Aikawa, S.-H. Ho, A. Nakanishi, J.-S. Chang, T. Hasunuma, and A. Kondo, “Improving polyglucan production in cyanobacteria and microalgae via cultivation design and metabolic engineering,” Biotechnol. J. 10(6), 886–898 (2015).
[Crossref]

P. Zhang, L. Ren, X. Zhang, Y. Shan, Y. Wang, Y. Ji, H. Yin, W. E. Huang, J. Xu, and B. Ma, “Raman-Activated Cell Sorting Based on Dielectrophoretic Single-Cell Trap and Release,” Anal. Chem. 87(4), 2282–2289 (2015).
[Crossref]

2014 (1)

A. Joseph, S. Aikawa, K. Sasaki, F. Matsuda, T. Hasunuma, and A. Kondo, “Increased biomass production and glycogen accumulation in apcE gene deleted Synechocystis sp. PCC 6803,” AMB Express 4(1), 17 (2014).
[Crossref]

2013 (3)

G. K. Kumaraswamy, T. Guerra, X. Qian, S. Zhang, D. A. Bryant, and G. C. Dismukes, “Reprogramming the glycolytic pathway for increased hydrogen production in cyanobacteria: metabolic engineering of NAD+-dependent GAPDH,” Energy Environ. Sci. 6(12), 3722–3731 (2013).
[Crossref]

C.-Y. Chen, X.-Q. Zhao, H.-W. Yen, S.-H. Ho, C.-L. Cheng, D.-J. Lee, F.-W. Bai, and J.-S. Chang, “Microalgae-based carbohydrates for biofuel production,” Biochem. Eng. J. 78, 1–10 (2013).
[Crossref]

T. Watanabe, R. Shimada, A. Matsuyama, M. Yuasa, H. Sawamura, E. Yoshida, and K. Suzuki, “Antitumor activity of the β-glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice,” Food Funct. 4(11), 1685–1690 (2013).
[Crossref]

2012 (1)

C. González-Fernández and M. Ballesteros, “Linking microalgae and cyanobacteria culture conditions and key-enzymes for carbohydrate accumulation,” Biotechnol. Adv. 30(6), 1655–1661 (2012).
[Crossref]

2011 (1)

A. Demirbas and M. Fatih Demirbas, “Importance of algae oil as a source of biodiesel,” Energy Convers. Manage. 52(1), 163–170 (2011).
[Crossref]

2010 (2)

M. E. Lidstrom and M. C. Konopka, “The role of physiological heterogeneity in microbial population behavior,” Nat. Chem. Biol. 6(10), 705–712 (2010).
[Crossref]

P. Paszek, S. Ryan, L. Ashall, K. Sillitoe, C. V. Harper, D. G. Spiller, D. A. Rand, and M. R. H. White, “Population robustness arising from cellular heterogeneity,” Proc. Natl. Acad. Sci. 107(25), 11644–11649 (2010).
[Crossref]

2005 (1)

C. Furusawa, T. Suzuki, A. Kashiwagi, T. Yomo, and K. Kaneko, “Ubiquity of log-normal distributions in intra-cellular reaction dynamics,” Biophysics (Biophys. Soc. Jpn.) 1, 25–31 (2005).
[Crossref]

2001 (2)

E. Limpert, W. A. Stahel, and M. Abbt, “Log-normal Distributions across the Sciences: Keys and Clues,” BioScience 51(5), 341–352 (2001).
[Crossref]

L. Barsanti, R. Vismara, V. Passarelli, and P. Gualtieri, “Paramylon (β-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis. Effects of growth conditions,” J. Appl. Phycol. 13(1), 59–65 (2001).
[Crossref]

2000 (1)

A. Álvarez-Barrientos, J. Arroyo, R. Cantón, C. Nombela, and M. Sánchez-Pérez, “Applications of flow cytometry to clinical microbiology,” Clin. Microbiol. Rev. 13(2), 167–195 (2000).
[Crossref]

1999 (1)

S. C. Feldman, S. Reynaldi, C. A. Stortz, A. S. Cerezo, and E. B. Damonte, “Antiviral properties of fucoidan fractions from Leathesia difformis,” Phytomedicine 6(5), 335–340 (1999).
[Crossref]

1982 (1)

Y. Oda, Y. Nakano, and S. Kitaoka, “Utilization and Toxicity of Exogenous Amino Acids in Euglena gracilis,” Microbiology (London, U. K.) 128(4), 853–858 (1982).
[Crossref]

1967 (1)

L. E. Koren and S. H. Hutner, “High-yield media for photosynthesizing Euglena gracilis Z,” J. Protozool. 14, 17 (1967).

Abbt, M.

E. Limpert, W. A. Stahel, and M. Abbt, “Log-normal Distributions across the Sciences: Keys and Clues,” BioScience 51(5), 341–352 (2001).
[Crossref]

Abe, T.

K. Yamada, H. Suzuki, T. Takeuchi, Y. Kazama, S. Mitra, T. Abe, K. Goda, K. Suzuki, and O. Iwata, “Efficient selective breeding of live oil-rich Euglena gracilis with fluorescence-activated cell sorting,” Sci. Rep. 6(1), 26327 (2016).
[Crossref]

Agusti, S.

S. Kottuparambil, R. L. Thankamony, and S. Agusti, “Euglena as a potential natural source of value-added metabolites. A review,” Algal Res. 37, 154–159 (2019).
[Crossref]

Aikawa, S.

S. Aikawa, S.-H. Ho, A. Nakanishi, J.-S. Chang, T. Hasunuma, and A. Kondo, “Improving polyglucan production in cyanobacteria and microalgae via cultivation design and metabolic engineering,” Biotechnol. J. 10(6), 886–898 (2015).
[Crossref]

A. Joseph, S. Aikawa, K. Sasaki, F. Matsuda, T. Hasunuma, and A. Kondo, “Increased biomass production and glycogen accumulation in apcE gene deleted Synechocystis sp. PCC 6803,” AMB Express 4(1), 17 (2014).
[Crossref]

Álvarez-Barrientos, A.

A. Álvarez-Barrientos, J. Arroyo, R. Cantón, C. Nombela, and M. Sánchez-Pérez, “Applications of flow cytometry to clinical microbiology,” Clin. Microbiol. Rev. 13(2), 167–195 (2000).
[Crossref]

Arai, F.

A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
[Crossref]

K. Hiramatsu, T. Ideguchi, Y. Yonamine, S. Lee, Y. Luo, K. Hashimoto, T. Ito, M. Hase, J.-W. Park, Y. Kasai, S. Sakuma, T. Hayakawa, F. Arai, Y. Hoshino, and K. Goda, “High-throughput label-free molecular fingerprinting flow cytometry,” Sci. Adv. 5(1), eaau0241 (2019).
[Crossref]

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
[Crossref]

Arroyo, J.

A. Álvarez-Barrientos, J. Arroyo, R. Cantón, C. Nombela, and M. Sánchez-Pérez, “Applications of flow cytometry to clinical microbiology,” Clin. Microbiol. Rev. 13(2), 167–195 (2000).
[Crossref]

Ashall, L.

P. Paszek, S. Ryan, L. Ashall, K. Sillitoe, C. V. Harper, D. G. Spiller, D. A. Rand, and M. R. H. White, “Population robustness arising from cellular heterogeneity,” Proc. Natl. Acad. Sci. 107(25), 11644–11649 (2010).
[Crossref]

Bai, F.-W.

C.-Y. Chen, X.-Q. Zhao, H.-W. Yen, S.-H. Ho, C.-L. Cheng, D.-J. Lee, F.-W. Bai, and J.-S. Chang, “Microalgae-based carbohydrates for biofuel production,” Biochem. Eng. J. 78, 1–10 (2013).
[Crossref]

Bajhaiya, A. K.

A. K. Bajhaiya, J. Ziehe Moreira, and J. K. Pittman, “Transcriptional Engineering of Microalgae: Prospects for High-Value Chemicals,” Trends Biotechnol. 35(2), 95–99 (2017).
[Crossref]

Ballesteros, M.

C. González-Fernández and M. Ballesteros, “Linking microalgae and cyanobacteria culture conditions and key-enzymes for carbohydrate accumulation,” Biotechnol. Adv. 30(6), 1655–1661 (2012).
[Crossref]

Barsanti, L.

L. Barsanti, R. Vismara, V. Passarelli, and P. Gualtieri, “Paramylon (β-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis. Effects of growth conditions,” J. Appl. Phycol. 13(1), 59–65 (2001).
[Crossref]

Bryant, D. A.

G. K. Kumaraswamy, T. Guerra, X. Qian, S. Zhang, D. A. Bryant, and G. C. Dismukes, “Reprogramming the glycolytic pathway for increased hydrogen production in cyanobacteria: metabolic engineering of NAD+-dependent GAPDH,” Energy Environ. Sci. 6(12), 3722–3731 (2013).
[Crossref]

Cantón, R.

A. Álvarez-Barrientos, J. Arroyo, R. Cantón, C. Nombela, and M. Sánchez-Pérez, “Applications of flow cytometry to clinical microbiology,” Clin. Microbiol. Rev. 13(2), 167–195 (2000).
[Crossref]

Cerezo, A. S.

S. C. Feldman, S. Reynaldi, C. A. Stortz, A. S. Cerezo, and E. B. Damonte, “Antiviral properties of fucoidan fractions from Leathesia difformis,” Phytomedicine 6(5), 335–340 (1999).
[Crossref]

Chang, J.-S.

T.-J. Chow, H.-Y. Su, T.-Y. Tsai, H.-H. Chou, T.-M. Lee, and J.-S. Chang, “Using recombinant cyanobacterium (Synechococcus elongatus) with increased carbohydrate productivity as feedstock for bioethanol production via separate hydrolysis and fermentation process,” Bioresour. Technol. 184, 33–41 (2015).
[Crossref]

S. Aikawa, S.-H. Ho, A. Nakanishi, J.-S. Chang, T. Hasunuma, and A. Kondo, “Improving polyglucan production in cyanobacteria and microalgae via cultivation design and metabolic engineering,” Biotechnol. J. 10(6), 886–898 (2015).
[Crossref]

C.-Y. Chen, X.-Q. Zhao, H.-W. Yen, S.-H. Ho, C.-L. Cheng, D.-J. Lee, F.-W. Bai, and J.-S. Chang, “Microalgae-based carbohydrates for biofuel production,” Biochem. Eng. J. 78, 1–10 (2013).
[Crossref]

Chen, C.-Y.

C.-Y. Chen, X.-Q. Zhao, H.-W. Yen, S.-H. Ho, C.-L. Cheng, D.-J. Lee, F.-W. Bai, and J.-S. Chang, “Microalgae-based carbohydrates for biofuel production,” Biochem. Eng. J. 78, 1–10 (2013).
[Crossref]

Cheng, C.-L.

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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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K. Hiramatsu, T. Ideguchi, Y. Yonamine, S. Lee, Y. Luo, K. Hashimoto, T. Ito, M. Hase, J.-W. Park, Y. Kasai, S. Sakuma, T. Hayakawa, F. Arai, Y. Hoshino, and K. Goda, “High-throughput label-free molecular fingerprinting flow cytometry,” Sci. Adv. 5(1), eaau0241 (2019).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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S. C. Feldman, S. Reynaldi, C. A. Stortz, A. S. Cerezo, and E. B. Damonte, “Antiviral properties of fucoidan fractions from Leathesia difformis,” Phytomedicine 6(5), 335–340 (1999).
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T.-J. Chow, H.-Y. Su, T.-Y. Tsai, H.-H. Chou, T.-M. Lee, and J.-S. Chang, “Using recombinant cyanobacterium (Synechococcus elongatus) with increased carbohydrate productivity as feedstock for bioethanol production via separate hydrolysis and fermentation process,” Bioresour. Technol. 184, 33–41 (2015).
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Su, X.

X. Jing, H. Gou, Y. Gong, X. Su, L. Xu, Y. Ji, Y. Song, I. P. Thompson, J. Xu, and W. E. Huang, “Raman-activated cell sorting and metagenomic sequencing revealing carbon-fixing bacteria in the ocean,” Environ. Microbiol. 20(6), 2241–2255 (2018).
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A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
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N. Wang, B. Guan, Q. Kong, H. Sun, Z. Geng, and L. Duan, “Enhancement of astaxanthin production from Haematococcus pluvialis mutants by three-stage mutagenesis breeding,” J. Biotechnol. 236, 71–77 (2016).
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K. Yamada, H. Suzuki, T. Takeuchi, Y. Kazama, S. Mitra, T. Abe, K. Goda, K. Suzuki, and O. Iwata, “Efficient selective breeding of live oil-rich Euglena gracilis with fluorescence-activated cell sorting,” Sci. Rep. 6(1), 26327 (2016).
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Suzuki, K.

Y. Wakisaka, Y. Suzuki, O. Iwata, A. Nakashima, T. Ito, M. Hirose, R. Domon, M. Sugawara, N. Tsumura, H. Watarai, T. Shimobaba, K. Suzuki, K. Goda, and Y. Ozeki, “Probing the metabolic heterogeneity of live Euglena gracilis with stimulated Raman scattering microscopy,” Nat. Microbiol. 1(10), 16124 (2016).
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K. Yamada, H. Suzuki, T. Takeuchi, Y. Kazama, S. Mitra, T. Abe, K. Goda, K. Suzuki, and O. Iwata, “Efficient selective breeding of live oil-rich Euglena gracilis with fluorescence-activated cell sorting,” Sci. Rep. 6(1), 26327 (2016).
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T. Watanabe, R. Shimada, A. Matsuyama, M. Yuasa, H. Sawamura, E. Yoshida, and K. Suzuki, “Antitumor activity of the β-glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice,” Food Funct. 4(11), 1685–1690 (2013).
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Suzuki, N.

A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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C. Furusawa, T. Suzuki, A. Kashiwagi, T. Yomo, and K. Kaneko, “Ubiquity of log-normal distributions in intra-cellular reaction dynamics,” Biophysics (Biophys. Soc. Jpn.) 1, 25–31 (2005).
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Suzuki, Y.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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Y. Wakisaka, Y. Suzuki, O. Iwata, A. Nakashima, T. Ito, M. Hirose, R. Domon, M. Sugawara, N. Tsumura, H. Watarai, T. Shimobaba, K. Suzuki, K. Goda, and Y. Ozeki, “Probing the metabolic heterogeneity of live Euglena gracilis with stimulated Raman scattering microscopy,” Nat. Microbiol. 1(10), 16124 (2016).
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Takeuchi, T.

K. Yamada, H. Suzuki, T. Takeuchi, Y. Kazama, S. Mitra, T. Abe, K. Goda, K. Suzuki, and O. Iwata, “Efficient selective breeding of live oil-rich Euglena gracilis with fluorescence-activated cell sorting,” Sci. Rep. 6(1), 26327 (2016).
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Tanaka, Y.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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Tezuka, H.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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X. Jing, H. Gou, Y. Gong, X. Su, L. Xu, Y. Ji, Y. Song, I. P. Thompson, J. Xu, and W. E. Huang, “Raman-activated cell sorting and metagenomic sequencing revealing carbon-fixing bacteria in the ocean,” Environ. Microbiol. 20(6), 2241–2255 (2018).
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Toyokawa, C.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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Tsai, T.-Y.

T.-J. Chow, H.-Y. Su, T.-Y. Tsai, H.-H. Chou, T.-M. Lee, and J.-S. Chang, “Using recombinant cyanobacterium (Synechococcus elongatus) with increased carbohydrate productivity as feedstock for bioethanol production via separate hydrolysis and fermentation process,” Bioresour. Technol. 184, 33–41 (2015).
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Tsumura, N.

Y. Wakisaka, Y. Suzuki, O. Iwata, A. Nakashima, T. Ito, M. Hirose, R. Domon, M. Sugawara, N. Tsumura, H. Watarai, T. Shimobaba, K. Suzuki, K. Goda, and Y. Ozeki, “Probing the metabolic heterogeneity of live Euglena gracilis with stimulated Raman scattering microscopy,” Nat. Microbiol. 1(10), 16124 (2016).
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Uemura, S.

A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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Vismara, R.

L. Barsanti, R. Vismara, V. Passarelli, and P. Gualtieri, “Paramylon (β-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis. Effects of growth conditions,” J. Appl. Phycol. 13(1), 59–65 (2001).
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Wakisaka, Y.

Y. Wakisaka, Y. Suzuki, O. Iwata, A. Nakashima, T. Ito, M. Hirose, R. Domon, M. Sugawara, N. Tsumura, H. Watarai, T. Shimobaba, K. Suzuki, K. Goda, and Y. Ozeki, “Probing the metabolic heterogeneity of live Euglena gracilis with stimulated Raman scattering microscopy,” Nat. Microbiol. 1(10), 16124 (2016).
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Wang, N.

N. Wang, B. Guan, Q. Kong, H. Sun, Z. Geng, and L. Duan, “Enhancement of astaxanthin production from Haematococcus pluvialis mutants by three-stage mutagenesis breeding,” J. Biotechnol. 236, 71–77 (2016).
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Wang, Y.

P. Zhang, L. Ren, X. Zhang, Y. Shan, Y. Wang, Y. Ji, H. Yin, W. E. Huang, J. Xu, and B. Ma, “Raman-Activated Cell Sorting Based on Dielectrophoretic Single-Cell Trap and Release,” Anal. Chem. 87(4), 2282–2289 (2015).
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Watanabe, T.

T. Watanabe, R. Shimada, A. Matsuyama, M. Yuasa, H. Sawamura, E. Yoshida, and K. Suzuki, “Antitumor activity of the β-glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice,” Food Funct. 4(11), 1685–1690 (2013).
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Watarai, H.

Y. Wakisaka, Y. Suzuki, O. Iwata, A. Nakashima, T. Ito, M. Hirose, R. Domon, M. Sugawara, N. Tsumura, H. Watarai, T. Shimobaba, K. Suzuki, K. Goda, and Y. Ozeki, “Probing the metabolic heterogeneity of live Euglena gracilis with stimulated Raman scattering microscopy,” Nat. Microbiol. 1(10), 16124 (2016).
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White, M. R. H.

P. Paszek, S. Ryan, L. Ashall, K. Sillitoe, C. V. Harper, D. G. Spiller, D. A. Rand, and M. R. H. White, “Population robustness arising from cellular heterogeneity,” Proc. Natl. Acad. Sci. 107(25), 11644–11649 (2010).
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Xu, J.

X. Jing, H. Gou, Y. Gong, X. Su, L. Xu, Y. Ji, Y. Song, I. P. Thompson, J. Xu, and W. E. Huang, “Raman-activated cell sorting and metagenomic sequencing revealing carbon-fixing bacteria in the ocean,” Environ. Microbiol. 20(6), 2241–2255 (2018).
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P. Zhang, L. Ren, X. Zhang, Y. Shan, Y. Wang, Y. Ji, H. Yin, W. E. Huang, J. Xu, and B. Ma, “Raman-Activated Cell Sorting Based on Dielectrophoretic Single-Cell Trap and Release,” Anal. Chem. 87(4), 2282–2289 (2015).
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Xu, L.

X. Jing, H. Gou, Y. Gong, X. Su, L. Xu, Y. Ji, Y. Song, I. P. Thompson, J. Xu, and W. E. Huang, “Raman-activated cell sorting and metagenomic sequencing revealing carbon-fixing bacteria in the ocean,” Environ. Microbiol. 20(6), 2241–2255 (2018).
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Yalikun, Y.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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Yamada, K.

K. Yamada, H. Suzuki, T. Takeuchi, Y. Kazama, S. Mitra, T. Abe, K. Goda, K. Suzuki, and O. Iwata, “Efficient selective breeding of live oil-rich Euglena gracilis with fluorescence-activated cell sorting,” Sci. Rep. 6(1), 26327 (2016).
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Yamada, M.

A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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Yamagishi, M.

N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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Yamano, T.

A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
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N. Nitta, T. Sugimura, A. Isozaki, H. Mikami, K. Hiraki, S. Sakuma, T. Iino, F. Arai, T. Endo, Y. Fujiwaki, H. Fukuzawa, M. Hase, T. Hayakawa, K. Hiramatsu, Y. Hoshino, M. Inaba, T. Ito, H. Karakawa, Y. Kasai, K. Koizumi, S. Lee, C. Lei, M. Li, T. Maeno, S. Matsusaka, D. Murakami, A. Nakagawa, Y. Oguchi, M. Oikawa, T. Ota, K. Shiba, H. Shintaku, Y. Shirasaki, K. Suga, Y. Suzuki, N. Suzuki, Y. Tanaka, H. Tezuka, C. Toyokawa, Y. Yalikun, M. Yamada, M. Yamagishi, T. Yamano, A. Yasumoto, Y. Yatomi, M. Yazawa, D. Di Carlo, Y. Hosokawa, S. Uemura, Y. Ozeki, and K. Goda, “Intelligent Image-Activated Cell Sorting,” Cell 175(1), 266–276.e13 (2018).
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Yasumoto, A.

A. Isozaki, H. Mikami, K. Hiramatsu, S. Sakuma, Y. Kasai, T. Iino, T. Yamano, A. Yasumoto, Y. Oguchi, N. Suzuki, Y. Shirasaki, T. Endo, T. Ito, K. Hiraki, M. Yamada, S. Matsusaka, T. Hayakawa, H. Fukuzawa, Y. Yatomi, F. Arai, D. Di Carlo, A. Nakagawa, Y. Hoshino, Y. Hosokawa, S. Uemura, T. Sugimura, Y. Ozeki, N. Nitta, and K. Goda, “A practical guide to intelligent image-activated cell sorting,” Nat. Protoc. 14(8), 2370–2415 (2019).
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Figures (3)

Fig. 1.
Fig. 1. Large-scale analysis of numerous single live E. gracilis cells. A: Setup of the high-throughput broadband FT-CARS flow cytometer. B: Image of E. gracilis cells. C: Procedure of preparing E. gracilis cells.
Fig. 2.
Fig. 2. Time-dependent change of the averaged Raman spectral profiles (N = 10,000 for each condition). A: Raman spectrum of paramylon particles (top). Averaged Raman spectra of E. gracilis cells 1-25 days after the replacement of the culture (bottom). The asterisk (*) indicates the artificial peaks originating from the acoustic wave. B: Time-dependent changes of Raman intensities at 1092, 604 and 428 cm−1 (assignable to paramylon), 1149 cm−1 (unknown), and 1003 cm−1 (assignable to proteins).
Fig. 3.
Fig. 3. Statistical analysis of bioproducts in E. gracilis cells. A: Scatter plots of E. gracilis cells 1-25 days after the replacement of the culture in 998- and 1092-cm−1 Raman intensities. B: Raman spectra of single E. gracilis cells under different conditions. Corresponding plots in the scatter plots are indicated by the arrows. C: Histograms of single E. gracilis cells in paramylon content at different points in time. The solid curves are probability density functions modeled by lognormal functions convoluted by a Gaussian function. D: Extracted log-normal distributions by the fitting analysis in C. E: Time-dependent changes of the geometric mean ${\bar{x}^\ast }$ and multiplicative standard deviation ${s^\ast }$.