Monitoring the photosynthetic activity at single-cell level in Haematococcus lacustris

. 2023 ; 61 (4) : 473-482. [epub] 20231218

Status PubMed-not-MEDLINE Jazyk angličtina Země Česko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39649488

Haematococcus lacustris is an important species of green algae because it produces the high-value carotenoid astaxanthin. Astaxanthin production is enhanced by various stress conditions causing the transformation of green vegetative cells to red cells with high amounts of astaxanthin, which plays various photoprotective and antioxidant roles. Although intensive research has been conducted to reveal the regulation of astaxanthin production, the photosynthetic capacity of the various cell forms is unresolved at the single-cell level. In this work, we characterized the photosynthetic and morphological changes of Haematococcus cells, using a combination of microfluidic tools and microscopic chlorophyll fluorescence imaging. We found marked but reversible changes in the variable chlorophyll fluorescence signatures upon the transformation of green cells to red cells, and we propose that the photosynthetic activity as revealed by single-cell chlorophyll fluorescence kinetics serves as a useful phenotypic marker of the different cell forms of Haematococcus.

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Baker N.R.: Chlorophyll fluorescence: A probe of photosynthesis in vivo. – Annu. Rev. Plant Biol. 59: 89-113, 2008. 10.1146/annurev.arplant.59.032607.092759 PubMed DOI

Bashir F., Kovács S., Ábrahám Á. et al.: Viable protoplast formation of the coral endosymbiont alga Symbiodinium spp. in a microfluidics platform. – Lab Chip 22: 2986-2999, 2022. 10.1039/D2LC00130F PubMed DOI

Borowitzka M.A.: High-value products from microalgae – their development and commercialisation. – J. Appl. Phycol. 25: 743-756, 2013. 10.1007/s10811-013-9983-9 DOI

Boussiba S.: Carotenogenesis in the green alga Haematococcus pluvialis: Cellular physiology and stress response. – Physiol. Plantarum 108: 111-117, 2000. 10.1034/j.1399-3054.2000.108002111.x DOI

Brestic M., Zivcak M.: PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. – In: Rout G.R., Das A.B. (ed.): Molecular Stress Physiology of Plants. Pp. 87-131. Springer, India: 2013. 10.1007/978-81-322-0807-5_4 DOI

Chekanov K., Lukyanov A., Boussiba S. et al.: Modulation of photosynthetic activity and photoprotection in Haematococcus pluvialis cells during their conversion into haematocysts and back. – Photosynth. Res. 128: 313-323, 2016. 10.1007/s11120-016-0246-x PubMed DOI

Cheng X., Qi Z., Burdyny T. et al.: Low pressure supercritical CO2 extraction of astaxanthin from Haematococcus pluvialis demonstrated on a microfluidic chip. – Bioresource Technol. 250: 481-485, 2018. 10.1016/j.biortech.2017.11.070 PubMed DOI

Deák Z., Sass L., Kiss É. et al., Vass I.: Characterization of wave phenomena in the relaxation of flash-induced chlorophyll fluorescence yield in cyanobacteria. – BBA-Bioenergetics 1837: 1522-1532, 2014. 10.1016/j.bbabio.2014.01.003 PubMed DOI

Fratamico A., Tocquin P., Franck F.: The chlorophyll a fluorescence induction curve in the green microalga Haematococcus pluvialis: further insight into the nature of the P–S–M fluctuation and its relationship with the “low-wave” phenomenon at steady-state. – Photosynth. Res. 128: 271-285, 2016. 10.1007/s11120-016-0241-2 PubMed DOI

Hagen C., Bornman J.F., Braune W.: Reversible lowering of modulated chlorophyll fluorescence after saturating flashes in Haematococcus lacustris (Volvocales) at room temperature. – Physiol. Plantarum 86: 593-599, 1992. 10.1111/j.1399-3054.1992.tb02175.x DOI

Kakizono T., Kobayashi M., Nagai S.: Effect of carbon/nitrogen ratio on encystment accompanied with astaxanthin formation in a green alga, Haematococcus pluvialis. – J. Ferment. Bioeng. 74: 403-405, 1992. 10.1016/0922-338X(92)90041-R DOI

Kalaji H.M., Schansker G., Ladle R.J. et al.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. – Photosynth. Res. 122: 121-158, 2014. 10.1007/s11120-014-0024-6 PubMed DOI PMC

Kobayashi M., Kurimura Y., Kakizono T. et al.: Morphological changes in the life cycle of the green alga Haematococcus pluvialis. – J. Ferment. Bioeng. 84: 94-97, 1997. 10.1016/S0922-338X(97)82794-8 DOI

Krishna P.S., Morello G., Mamedov F.: Characterization of the transient fluorescence wave phenomenon that occurs during H2 production in Chlamydomonas reinhardtii. – J. Exp. Bot. 70: 6321-6336, 2019. 10.1093/jxb/erz380 PubMed DOI PMC

Kwak H.S., Kim J.Y.H., Sim S.J.: A microreactor system for cultivation of Haematococcus pluvialis and astaxanthin production. – J. Nanosci. Nanotechnol. 15: 1618-1623, 2015. 10.1166/jnn.2015.9321 PubMed DOI

Larcher W., Neuner G.: Cold-induced sudden reversible lowering of in vivo chlorophyll fluorescence after saturating light pulses: A sensitive marker for chilling susceptibility. – Plant Physiol. 89: 740-742, 1989. 10.1104/pp.89.3.740 PubMed DOI PMC

Leu S., Boussiba S.: Advances in the production of high-value products by microalgae. – Ind. Biotechnol. 10: 169-183, 2014. 10.1089/ind.2013.0039 DOI

Mascia F., Girolomoni L., Alcocer M.J.P. et al.: Functional analysis of photosynthetic pigment binding complexes in the green alga Haematococcus pluvialis reveals distribution of astaxanthin in Photosystems. – Sci. Rep.-UK 7: 16319, 2017. 10.1038/s41598-017-16641-6 PubMed DOI PMC

Mohammad Aslam S., Patil P.P., Vass I., Szabó M.: Heat-induced photosynthetic responses of Symbiodiniaceae revealed by flash-induced fluorescence relaxation kinetics. – Front. Mar. Sci. 9: 932355, 2022. 10.3389/fmars.2022.932355 DOI

Munekage Y., Hashimoto M., Miyake C. et al.: Cyclic electron flow around photosystem I is essential for photosynthesis. – Nature 429: 579-582, 2004. 10.1038/nature02598 PubMed DOI

Patil P.P., Mohammad Aslam S., Vass I., Szabó M.: Characterization of the wave phenomenon of flash-induced chlorophyll fluorescence in Chlamydomonas reinhardtii. – Photosynth. Res. 152: 235-244, 2022b. 10.1007/s11120-022-00900-3 PubMed DOI PMC

Patil P.P., Vass I., Szabó M.: Characterization of the wave phenomenon in flash-induced fluorescence relaxation and its application to study cyclic electron pathways in microalgae. – Int. J. Mol. Sci. 23: 4927, 2022a. 10.3390/ijms23094927 PubMed DOI PMC

Ralph P.J., Gademann R.: Rapid light curves: A powerful tool to assess photosynthetic activity. – Aquat. Bot. 82: 222-237, 2005. 10.1016/j.aquabot.2005.02.006 DOI

Roach T., Fambri A., Ballesteros D.: Humidity and light modulate oxygen-induced viability loss in dehydrated Haematococcus lacustris cells. – Oxygen 2: 503-517, 2022. 10.3390/oxygen2040033 DOI

Schreiber U.: Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: An overview. – In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 279-319. Springer, Dordrecht: 2004. 10.1007/978-1-4020-3218-9_11 DOI

Scibilia L., Girolomoni L., Berteotti S. et al.: Photosynthetic response to nitrogen starvation and high light in Haematococcus pluvialis. – Algal Res. 12: 170-181, 2015. 10.1016/j.algal.2015.08.024 DOI

Shikanai T., Endo T., Hashimoto T. et al.: Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. – PNAS 95: 9705-9709, 1998. 10.1073/pnas.95.16.9705 PubMed DOI PMC

Sipka G., Magyar M., Mezzetti A. et al.: Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center. – Plant Cell 33: 1286-1302, 2021. 10.1093/plcell/koab008 PubMed DOI PMC

Solovchenko A., Lukyanov A., Vasilieva S., Lobakova E.: Chlorophyll fluorescence as a valuable multitool for microalgal biotechnology. – Biophys. Rev. 14: 973-983, 2022. 10.1007/s12551-022-00951-9 PubMed DOI PMC

Solovchenko A.E.: Recent breakthroughs in the biology of astaxanthin accumulation by microalgal cell. – Photosynth. Res. 125: 437-449, 2015. 10.1007/s11120-015-0156-3 PubMed DOI

Széles E., Kuntam S., Vidal-Meireles A. et al.: Single-cell microfluidics in combination with chlorophyll a fluorescence measurements to assess the lifetime of the Chlamydomonas PSBO protein. – Photosynthetica 61: 417-424, 2023. 10.32615/ps.2023.028 DOI

Széles E., Nagy K., Ábrahám Á. et al.: Microfluidic platforms designed for morphological and photosynthetic investigations of Chlamydomonas reinhardtii on a single-cell level. – Cells 11: 285, 2022. 10.3390/cells11020285 PubMed DOI PMC

Tan S., Cunningham Jr. F.X., Youmans M. et al.: Cytochrome f loss in astaxanthin-accumulating red cells of Haematococcus pluvialis (Chlorophyceae): comparison of photosynthetic activity, photosynthetic enzymes, and thylakoid membrane polypeptides in red and green cells. – J. Phycol. 31: 897-905, 1995. 10.1111/j.0022-3646.1995.00897.x DOI

Tsuyama M., Shibata M., Kawazu T., Kobayashi Y.: An analysis of the mechanism of the low-wave phenomenon of chlorophyll fluorescence. – Photosynth. Res. 81: 67-76, 2004. 10.1023/B:PRES.0000028394.60328.b5 PubMed DOI

Xyländer M., Hagen C.: ‘Low-waves’ in chlorophyll fluorescence kinetics indicate deprivation of bicarbonate. – Photosynth. Res. 72: 255-262, 2002. 10.1023/a:1019864623049 PubMed DOI

Yamori W., Shikanai T., Makino A.: Photosystem I cyclic electron flow via chloroplast NADH dehydrogenase-like complex performs a physiological role for photosynthesis at low light. – Sci. Rep.-UK 5: 13908, 2015. 10.1038/srep13908 PubMed DOI PMC

Zhang L., Su F., Zhang C. et al.: Changes of photosynthetic behaviors and photoprotection during cell transformation and astaxanthin accumulation in Haematococcus pluvialis grown outdoors in tubular photobioreactors. – Int. J. Mol. Sci. 18: 33, 2017. 10.3390/ijms18010033 PubMed DOI PMC

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