Monitoring the photosynthetic activity at single-cell level in Haematococcus lacustris
Status PubMed-not-MEDLINE Jazyk angličtina Země Česko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
39649488
PubMed Central
PMC11586838
DOI
10.32615/ps.2023.042
PII: PS61473
Knihovny.cz E-zdroje
- Klíčová slova
- Haematococcus lacustris, chlorophyll fluorescence, photoprotection, photosynthesis, photosystem II,
- Publikační typ
- časopisecké články MeSH
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.
Climate Change Cluster University of Technology Sydney Ultimo NSW 2007 Australia
Doctoral School of Multidisciplinary Medical Sciences University of Szeged 6720 Szeged Hungary
Institute of Biophysics HUN REN Biological Research Centre 6726 Szeged Hungary
Institute of Plant Biology HUN REN Biological Research Centre 6726 Szeged Hungary
Zobrazit více v PubMed
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