Screening of growth phases of Antarctic algae and cyanobacteria cultivated on agar plates by chlorophyll fluorescence imaging

Vol.9,No.2(2019)

Abstract

Recently, chlorophyll fluorescence imaging is frequently used non-invasive method to monitor the metabolic state and photosynthetic activities of vascular plants and other autotrophic organisms. In our study, we used the measurements of chlorophyll fluorescence kinetics to follow the development of culture of Antarctic algae (Macrochloris rubrioleum, Zygnema sp.) and cyanobacteria (Hassalia antarctica, Nostoc commune). On the cultures grown on agar plates, Bold´s Basal Medium (BBM), slow Kautsky kinetics supplemented with saturation pulses were measured repeatedly in a week interval. On the kinetics, typical points (OPSMT) were distinguished and species-specific and time of cultivation-dependent differences in shape of the OPSMT kinetics evaluated. We tested sensitivity of various chlorophyll fluorescence parameters to cultivation time on agar plates. In the algae, the most pronounced changes were the decrease in maximum quantum yield of photosystem II (FV/FM) and quenching of basal chlorophyll fluorescence qF0 (M. rubrioleum, Zygnema sp.). In cyanobacteria, chlorophyll fluorescence parameters did not show clear trends with the time of cultivation. F0 quenching (qF0) reached positive values in H. antarctica, while it was negative in N. commune. In both cases, however, qF0 showed an increase with cultivation time. The differences are discussed as well as the potential of the emerging area of the application of chlorophyll fluorescence imaging for evaluation of photosynthetic performance of algal/cyanobacterial cultures on agar plates.


Keywords:
microalgae; in vitro cultivation; slow Kautsky kinetics; OPSMT
References
<p class="msolistparagraph0" style="text-align: justify; text-indent: -11.35pt; line-height: normal; margin-left: 11.35pt; margin-right: 0cm; margin-top: 0cm; margin-bottom: .0001pt"> <span lang="EN-GB" style="font-size: 9.0pt; font-family: 'Times New Roman',serif; font-variant: small-caps"> Allen, J. F.</span><span lang="EN-GB" style="font-size: 9.0pt; font-family: 'Times New Roman',serif"> (1992): Protein phosphorylation in regulation of photosynthesis. <i> Biochimica et Biophysica Acta (BBA) - Bioenergetics</i>, 1098(3): 275-335.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Alonso, M. C.</span><span lang="EN-GB" style="font-size: 9.0pt"> (2018): Changes in chlorophyll fluorescence parameters during desiccation and osmotic stress of <i>Hassallia antarctica</i> culture. <i>Czech Polar Reports</i>, 8: 198-207.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Bilger, W., Schreiber, U.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1986): Energy-dependent quenching of dark-level chlorophyll fluorescence in intact leaves. <i>Photosynthesis Research</i>, 10(3): 303-308.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-US" style="font-size: 9.0pt; font-variant: small-caps"> Buchanan, B. B., Balmer, Y.</span><span lang="EN-US" style="font-size: 9.0pt"> (2005). </span><span lang="EN-GB" style="font-size: 9.0pt">Redox regulation: A broadening horizon. <i>Annual Review of Plant Biology</i>,<i> </i>56: 187-220.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Fujimori, T., Higuchi, M., Sato, H., Aiba, H., Muramatsu, M., Hihara, Y.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Sonoike, K.</span> (2005): The mutant of sll1961, which encodes a putative transcriptional regulator, has a defect in regulation of photosystem stoichiometry in the cyanobacterium <i>Synechocystis</i> sp. PCC 6803. <i>Plant Physiology</i>, 139(1): 408-416.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Gavel, A., Maršálek, B.</span><span lang="EN-GB" style="font-size: 9.0pt"> (2004): A novel approach for phytotoxicity assessment by ccd fluorescence immaging. <i>Environmental Toxicology</i>, 19: 429-432.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Govindjee </span><span lang="EN-GB" style="font-size: 9.0pt">(1995): Sixty-three years since Kautsky: chlorophyll a fluorescence. <i> Australian Journal of Plant Physiology</i>, 22(2): 131-160. </span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Hansen, U.P., Moldaenchke, C., Tabrizi, H.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Ramm, D</span>. (1993): The effect of transthylakoid proton uptake on cytosolic pH and the imbalance of ATP and NADPH/H<sup>+</sup> production as measured by CO<sub>2</sub> and light induced depolarisation of the plasmalemma, <i>Plant and Cell Physiology</i>, 34: 681-695.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Havaux, M.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1990): "Energy"-dependent quenching of chlorophyll fluorescence and thermal energy dissipation in intact leaves during induction of photosynthesis. <i>Photochemistry and Photobiology</i>, 51(4): 481-486.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Hodges, M., Barber, J.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1984): Analysis of chlorophyll fluorescence quenching by DBMIB as a means of investigating the consequences of thylakoid membrane phosphorylation. <i>Biochimica et Biophysica Acta (BBA) - Bioenergetics</i>, 767(1): 102-107.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Ireland, C. R., Baker, N. R.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant: small-caps">Long, S. P.</span> (1985): The role of carbon dioxide and oxygen in determining chlorophyll fluorescence quenching during leaf development. <i>Planta</i>, 165(4): 477-485.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Kaňa, R., Kotabová, E., Komárek, O., Šedivá, B., Papageorgiou, G. C., Govindjee</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Prášil, O.</span> (2012): The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. <i>Biochimica et Biophysica Acta</i>, 1817: 1237-1247.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span style="font-size:9.0pt;font-variant:small-caps">Kawasaki, Y., Nakada, T.</span><span style="font-size:9.0pt"> and <span style="font-variant: small-caps">Tomita, M.</span> (2015): Taxonomic revision of oil-producing green algae, <i>Chlorococcum oleofaciens</i> (Volvocales, Chlorophyceae), and its relatives. <i>Journal of Phycology</i>, 51, pg 1000-1016. (Corrigendum, 52:156-156).</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span style="font-size:9.0pt;font-variant:small-caps">Kodru, S., Malavath, T., Devadasu, E., Nellaepalli, S., Stirbet, A., Subramanyam, R.</span><span style="font-size:9.0pt"> and <span style="font-variant:small-caps">Govindjee</span> (2015): The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga <i>Chlamydomonas reinhardtii</i>. <i> Photosynthesis Research</i>, 125: 219-231.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span style="font-size:9.0pt;font-variant:small-caps">Komárek, O., Felcmanová, K., Šetlíková, E., Kotabová, E., Trtílek, M.</span><span style="font-size:9.0pt"> and <span style="font-variant:small-caps">Prášil, O.</span> (2010): Microscopic measurements of the chlorophyll <i>a</i> fluorescence kinetics. </span><i><span lang="EN-GB" style="font-size: 9.0pt">In</span></i><span lang="EN-GB" style="font-size: 9.0pt">: D. J. Suggett, M. A. Borowitzka, O. Prášil (eds.): Chlorophyll <i>a</i> fluorescence in aquatic sciences: Methods and Applications. Springer, pp. 91-101. </span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Krause, G. H</span><span lang="EN-GB" style="font-size: 9.0pt">. (1988): Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. <i>Physiologia Plantarum</i>, 74(3): 566-574.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Krause, G. H., Laasch, H.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1987): Photoinhibition of photosynthesis. Studies on mechanisms of damage and protection in chloroplasts. <i>In</i>: J. BIGGINS (eds.): <i> Progress in Photosynthesis Research</i>. Springer, Dordrecht, pp. 19-26.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Krause, G. H., Weis, E.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1991): Chlorophyll fluorescence and photosynthesis – the basics. <i> Annual Review of Plant Physiology and Plant Molecular Biology</i>, 42: 313-349.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Lazár, D.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1999): Chlorophyll <i>a</i> fluorescence induction. <i>Biochimica et Biophysica Acta</i>,<i> </i>1412(1): 1-28.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Lichtenthaler, H. K., Buschmann, C.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Knapp, M.</span> (2005): How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. <i>Photosynthetica</i>, 43: 379-393.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Marečková, M., Barták, M</span><span lang="EN-GB" style="font-size: 9.0pt">. and <span style="font-variant: small-caps">Hájek, J.</span> (2019): Temperature effects on photosynthetic performance of Antarctic lichen <i>Dermatocarpon polyphyllizum</i>: A chlorophyll fluorescence study. <i>Polar Biology</i>, 42: 685-701.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Mishra, A., Mishra, K. B., Höermiller, I. I., Heyer, A. G.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Nedbal, L.</span> (2011): Chlorophyll fluorescence emission as a reporter on cold tolerance in <i> Arabidopsis thaliana</i> accessions. <i>Plant Signaling and Behavior</i>, 6: 301-310.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Murchie, E.H., Lawson, T.</span><span lang="EN-GB" style="font-size: 9.0pt"> (2013): Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. <i>Journal of Experimental Botany</i>, 64: 3983-3998.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Noctor, G., Horton, P.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1990): Uncoupler titration of energy-dependent chlorophyll fluorescence quenching and Photosystem II Photochemical yield in intact pea chloroplasts. <i>Biochimica et Biophysica Acta (BBA) – Bioenergetics,</i> 1016(2): 228-234.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Ogawa, T.</span><span lang="EN-GB" style="font-size: 9.0pt"> (2017): Characteristics of photosynthesis in cyanobacteria probed by chlorophyll fluorescence measurements. Waseda University Graduate School of Advanced Science and Engineering Department of Integrative Bioscience and Biomedical Engineering Research on Plant Physiology and Biochemistry. 86 p.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Ozaki, H., Ikeuchi, M., Ogawa, T., Fukuzawa, H.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Sonoike, K.</span> (2007): Large-scale analysis of chlorophyll fluorescence kinetics in <i> Synechocystis</i> sp. PCC 6803: Identification of the factors involved in the modulation of photosystem stoichiometry. <i>Plant and Cell Physiology</i>, 48(3): 451-458.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Ozaki, H., Sonoike, K.</span><span lang="EN-GB" style="font-size: 9.0pt"> (2009): Quantitative analysis of the relationship between induction kinetics of chlorophyll fluorescence and function of genes in the cyanobacterium <i>Synechocystis</i> sp. PCC 6803. <i>Photosynthesis Research</i>, 101(1): 47-58.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Papageorgiou, G., Tsimili-Michael, M</span><span lang="EN-GB" style="font-size: 9.0pt">. and <span style="font-variant:small-caps">Stamatakis, K.</span> (2007): The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: A viewpoint. <i>Photosynthesis Research</i>, 94: 275-90.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Riznichenko, G., Lebedeva, G., Pogosyan, S., Sivchenko, M.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Rubin, A.</span> (1996): Fluorescence induction curves registered from individual microalgae cenobiums in the process of population growth. <i>Photosynthesis Research</i>, 49(2): 151-157.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Roháček, K., Barták, M</span><span lang="EN-GB" style="font-size: 9.0pt">. (1999): Technique of the modulated chlorophyll fluorescence: Basic concepts, useful parameters, and some applications. <i>Photosynthetica</i>, 37: 339-363.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Seaton, G. G. R., Walker, D. A.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1990): Chlorophyll fluorescence as a measure of photosynthetic carbon assimilation. <i>Proceedings of the Royal Society of London. Series B: Biological Sciences</i>, 242(1303): 29-35.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Stirbet, A., Govindjee</span><span lang="EN-GB" style="font-size: 9.0pt"> (2011): On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. <i>Journal of Photochemistry and Photobiology B: Biology</i>, 104(1-2):236-257. doi: 10.1016/j.jphotobiol.2010.12.010 </span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Tolleter, D. B., Ghysels, B., Alric, J., Petroutsos, D., Tolstygina, I., Krawietz, D., Happe, T., Auroy, P., Adriano, J. M., Beyly, A., Cuiné, S., Plet, J., Reiter, I. M., Genty, B., Cournac, L., Hippler, M.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Peltier, G</span>. (2011): Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in <i>Chlamydomonas reinhardtii</i>. <i>The Plant Cell</i>, 23(7): 2619-2630.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Walker, D. A.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1981): Secondary fluorescence kinetics of spinach leaves in relation to the onset of photosynthetic carbon assimilation. <i>Planta</i>, 143: 273-278.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Walker, D. A., Sivak, M. N., Prinsley, R. T.</span><span lang="EN-GB" style="font-size: 9.0pt"> and <span style="font-variant:small-caps">Cheesbrough, J. K.</span> (1983): Simultaneous measurement of oscillations in oxygen evolution and chlorophyll a fluorescence in leaf pieces. <i>Plant Physiology</i>, 73(3): 542-549.</span></p> <p class="MsoNormal" style="margin-left:11.35pt;text-align:justify;text-indent: -11.35pt"><span lang="EN-GB" style="font-size: 9.0pt; font-variant: small-caps"> Walker, D. A., Osmond, Ch. B.</span><span lang="EN-GB" style="font-size: 9.0pt"> (1986): Measurement of photosynthesis in vivo with a leaf disc electrode: correlations between light dependence of steady-state photosynthetic O<sub>2</sub> evolution and chlorophyll a fluorescence transients. <i>Proceedings of the Royal Society of London. Series B: Biological Sciences</i>, 227(1248): 267-280</span><span style="font-size:9.0pt">.</span>
Metrics

458

Views

90

PDF views