Photosynthetic efficiency of endosymbiotic algae of Paramecium bursaria originating from locations with cold and warm climates

• Autorzy: Możdżeń K. , Leśnicka P. Z. , Burnecki T. , Śliwińska-Wilczewska S. , Skoczowski A. , Greczek-Stachura M.

Identyfikatory

DOI

10.1515/ohs-2018-0019

• Języki publikacji: EN

Abstrakty

EN

Paramecium bursaria (Ciliophora) is a cosmopolitan unicellular organism that plays a significant role in aquatic ecosystems. P. bursaria contains symbiotic algae and this association is a mutual symbiosis. The aim of the present study was to determine the activity of photosystem II (PSII) in Chlorella sp. inside P. bursaria cells. Ciliates were incubated for 7 days at different temperatures from 6 to 18°C, under the circadian cycle: 12 h light/12 h dark, at light intensity of 200 μmol m^-2 s^-1

Słowa kluczowe

EN

chlorophyll a fluorescence; endosymbiotic Chlorella sp.; photosystem II; PSII; temperature

• Wydawca: Institute of Oceanography University of Gdańsk
• Czasopismo: Oceanological and Hydrobiological Studies
• Rocznik: 2018
• Tom: Vol. 47, No. 2
• Strony: 202--210
• Opis fizyczny: Bibliogr. 63 poz.

Twórcy

autor

Możdżeń K.

• Department of Plant Physiology, Institute of Biology, Pedagogical University of Cracow, ul. Podchorążych 2, 30-084 Kraków, Poland

autor

Leśnicka P. Z.

• Department of Plant Physiology, Institute of Biology, Pedagogical University of Cracow, ul. Podchorążych 2, 30-084 Kraków, Poland

autor

Burnecki T.

• Department of Plant Physiology, Institute of Biology, Pedagogical University of Cracow, ul. Podchorążych 2, 30-084 Kraków, Poland

autor

Śliwińska-Wilczewska S.

• Department of Marine Ecosystem Functioning, Institute of Oceanography, Faculty of Oceanography and Geography, University of Gdańsk, Al. M. Piłsudskiego 46, 81-378 Gdynia, Poland

autor

Skoczowski A.

• Department of Plant Physiology, Institute of Biology, Pedagogical University of Cracow, ul. Podchorążych 2, 30-084 Kraków, Poland

autor

Greczek-Stachura M.

• Department of Plant Physiology, Institute of Biology, Pedagogical University of Cracow, ul. Podchorążych 2, 30-084 Kraków, Poland

Bibliografia

• [1]. Allakhverdieva, S.I. & Murataa, N. (2004). Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim. Biophys. Acta. 1657: 23-32.
• [2]. Allen, J.F., Alexciev, K. & Håkansson, G. (1995). Photosynthesis: Regulation by redox signalling. Curr. Biol. 5: 869-872.
• [3]. Aro, E.M., Virgin, I. & Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta. 1143: 113-134.
• [4]. Bailey, S., Melis, A., Mackey, K.R., Cardol, P., Finazzi, G. et al. (2008). Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim. Biophys. Acta. 1777: 269-276.
• [5]. Berk, S.G., Parks, L.H. & Ting, R.S. (1991). Photoadaptation alters the ingestion rate of Paramecium bursaria, a mixotrophic ciliate. Appl. Environ. Microbiol. 57: 2312-2316.
• [6]. Büchel, C. & Wilhelm, C. (1993). In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: progress, problems and perspectives. Photochem. Photobiol. 58: 137-48.
• [7]. Butterwick, C., Heaney, S.I. & Talling, J.F. (2005). Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw. Biol. 50: 291-300.
• [8]. Carvalho, L., Miller, C.A., Scott, E.M., Geoffrey, A.C., Davies, P.S. et al. (2011). Cyanobacterial blooms: statistical models describing risk factors for national-scale lake assessment and lake management. Sci. Tot. Environ. 409: 5353-5358.
• [9]. Chemeris, Y.K., Koroľkov, N.S., Seifullina, N.K. & Rubin, A.B. (2004b). Changes in the contents of inactive complexes of photosystem II in Chlorella cells incubated in the light and darkness. Russ. J. Plant Physiol. 51: 287-293.
• [10]. Chemeris, Y.K., Shenderova, L.V., Venediktov, P.S. & Rubin, A.B. (2004a). Activation of chlororespiration increases chlorophyll fluorescence yield in Chlorella adapted to darkness at high temperature. Biol. Bull. 31: 143-150.
• [11]. Coutteau, P. (1996). Micro-algae. In P. Lavens, P. Sorgeloos (Eds.), Manual on the production and use of live food for aquaculture (pp. 7-48). Rome, FAO Fisheries Technical, FAO.
• [12]. Dau, H. (1994). Molecular mechanisms and quantitive models of variable photosystem II fluorescence. J. Photochem. Photobiol. 60: 1-23.
• [13]. Ferrante, A. & Maggiore, T. (2007). Chlorophyll a fluorescence measurements to evaluate storage time and temperature of Valeriana leafy vegetables. Postharvest Biol. Technol. 45: 73-80.
• [14]. Flameling, I.A. & Kromkamp, J. (1997). Photoacclimation of Scenedesmus protuberans (Chlorophyceae) to fluctuating irradiances simulating vertical mixing. J. Plankton. Res. 19: 1011-1024.
• [15]. Force, L., Critchley, C. & Van Rensen, J.J.S. (2003). New fluorescence parameters for monitoring photosynthesis in plants. The effect of illumination on the fluorescence parameters of the JIP-test. Photosynth. Res. 78: 17-33.
• [16]. Franklin, L.A., Levavasseur, G., Osmond, C.B., Henley, W.J. & Ramus, J. (1992). Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 186: 399-408.
• [17]. Germino, M.J. & Smith, W.K. (2000a). Differences in microsite, plant form, and low-temperature photoinhibition in alpine-plants. Arct. Ant. Alp. Res. 32: 388-396.
• [18]. Germino, M.J. & Smith, W.K. (2000b). High resistance to low-temperature photoinhibition in two alpine, snowbank species. Physiol. Plant. 110: 89-95.
• [19]. Gilstad, M., Johnsen, G. & Sakshang, E. (1993). Photosynthetic parameters, pigment composition and respiration rates of the marine diatom Skeletonema costatum grown in continuous light and a 12:12 light-dark cycle. J. Plankton. Res. 15: 939-951.
• [20]. Gómez, I., Figueroa, F.L., Sousa-Pinto, I., Viñegla, B., Perez-Rodriguez, E. et al. (2001). Effects of UV radiation and temperature on photosynthesis as measured by PAM fluorescence in the red alga Gelidium pulchellum (Turner) Kützing. Bot. Mar. 44: 9-16.
• [21]. Hill, R., Schreiber, U., Gademann, R., Larkum, A.W.D., Kühl, M. et al. (2004). Spatial heterogeneity of photosynthesis and the effect of temperature-induced bleaching conditions in three species of corals. Mar. Biol. 144: 633-640.
• [22]. Hoshina, R. & Imamura, N. (2009). Origins of algal symbionts of Paramecium bursaria. In M. Fujishima (Ed.), Endosymbionts in Paramecium (pp. 1-29). Springer-Verlag GmbH.
• [23]. Jena, S., Acharya, S. & Mohapatra, P.K. (2012). Variation in effects off our OP insecticides on photosynthetic pigment fluorescence of Chlorella vulgaris Beij. Ecotox. and Environ. Safe. 80: 111-117.
• [24]. Jiang, C.D., Jiang, G.M., Wang, X., Li, L-H., Biswas, D.K. et al. (2006). Increased photosynthetic activities and thermostability of photosystem II with leaf development of elm seedlings (Ulmus pumila) probed by the fast fluorescence rise OJIP. Environ. Exp. Bot. 58: 261-268.
• [25]. Kalaji, H.M., Carpentier, R., Allakhverdiev, S.I. & Bosa, K. (2012). Fluorescence parameters as early indicators of light stress in barley. J. Photoch. Photobiol. B. 112: 1-6.
• [26]. Krzemińska, I., Piasecka, A., Nosalewicz, A., Simionato D. & Wawrzykowski, J. (2015). Alterations of the lipid content and fatty acid profile of Chlorella protothecoides under different light intensities. Bioresource Technol. 196: 72-77.
• [27]. Leitsch, J., Schnettger, B., Critchley, C. & Krause G.H. (1994). Two mechanisms of recovery from photoinhibition in vivo: reactivation of photosystem II related and unrelated to D1-protein turnover. Planta 194: 15-21.
• [28]. Levasseur, M.E., Morissette, J.C. & Harrison, P.J. (1990). Effects of long-term exposure to low-temperature on the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae). J. Phycol. 26: 479-484.
• [29]. Lu, C.M. & Vonshak, A. (1999). Photoinhibition in outdoor Spirulina platensis cultures assessed by polyphasic chlorophyll fluorescence transients. J. Appl. Phycol. 11: 355-359.
• [30]. Lu, C.M. & Vonshak, A. (2002). Effect of salinity on photosystem II function in cyanobacterial Spirulina platensis cells. Physiol. Plant. 114: 405-413.
• [31]. Magnusson, G. (1997). Diurnal measurements of Fv/Fm used to improve productivity estimates in microalgae. Mar. Biol. 130: 203-208.
• [32]. Masojídek, J., Kopecky, J., Giannelli, L. & Torzillo, G. (2011). Productivity correlated to photobiochemical performance of Chlorella mass cultures grown outdoors in thin-layer cascades. J. Ind. Microbiol. Biotechnol. 38: 307-317.
• [33]. Maxwell, D.P., Falk, S., Trick, C.G. & Huner, N.PA. (1994). Growth at low temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol. 105: 535-543.
• [34]. Maxwell, K. & Johnson, G.N. (2000). Chlorophyll fluorescence a practical guide. J. Exp. Bot. 51: 659-668.
• [35]. Mishra, R.K. & Singhal G.S. (1992). Function of photosynthetic apparatus of intact wheat leaves under high light and heat stress and its relationship with peroxidation of thylakoid lipids. Plant Physiol. 98: 1-6.
• [36]. Morgan-Kiss, R.M., Ivanov, A.G., Williams, J., Khan. M. & Huner, N.P.A. (2002). Differential thermal effects on the energy distribution between photosystem II and photosystem I in thylakoid membranes of a psychrophillic and a mesophillic alga. Biochim. Biophys. Acta. 1561: 251-265.
• [37]. Mortain-Bertrand, A., Descolas-Gros, C. & Jupin, H. (1988). Pathway of dark inorganic carbon fixation in two species of diatoms: influence of light regime and regulator factors on diel variations. J. Plankton. Res. 10: 199-217.
• [38]. Murata, N., Takahashi, S., Nishiyama, Y. & Allakhverdiev, S.I. (2007). Photoinhibition of photosystem II under environmental stress. Biochim. Biophys. Acta 1767: 414-421.
• [39]. Murchie, E.H. & Lawson, T. (2013). Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J. Exp. Bot. 64(13): 3983-3998.
• [40]. Nishiyama, Y., Allakverdiev, S. & Murata, N. (2008). Regulation by environmental conditions of the repair of photosystem II in cyanobacteria. In B. Demming-Adams, W.W. Adams III & A.K. Matto (Eds.), Photoprotection, Photoinhibition Gene Regulation, and Environment (pp. 193-203). Dordrecht, Springer.
• [41]. Osmond, B., Schwartz, O. & Gunning, B. (1999). Photoinhibitory printing on leaves, visualised by chlorophyll fluorescence imaging and confocal microscopy, is due to diminished fluorescence from grana. Aust. J. Plant. Physiol. 26: 717-724.
• [42]. Oukarroum, A., Perreault, F. & Popovic, R. (2012). Interactive effects of temperature and copper on photosystem II photochemistry in Chlorella vulgaris. J. Photochem. Photobiol. B 110: 9-14.
• [43]. Pado, R. (1965). Mutual relations of protozooans and symbiotic algae in Paramecium bursaria.The influence of light on the groeth of symbionts. Folia Biol. 13: 173-182.
• [44]. Reisser, W. & Benseler, W. (1981). Comparative studies on photosynthetic enzymes of the symbiotic Chlorella from Paramecium bursaria and other symbiotic and nonsymbiotic Chlorella strains. Arch. Microbiol. 129(2): 178-180.
• [45]. Reisser, W. (1980). The metabolic interactions between Paramecium bursaria Ehrbg. and Chlorella spec. in the Paramecium bursaria-symbiosis III. The Influence of different CO2 concentrations and of glucose on the photosynthetic and respiratory capacity of the symbiotic unit. Arch. Microbiol. 125: 291-293.
• [46]. Saakov, V.S. (2002). High-temperature stress-related changes in the harmonics F0’, Fm’, and Fv of pulse-amplitude modulated fluorescence signals: locating thermal damage in reaction centers of photosystem II. Dokl. Biochem. Biophys. 382: 4-9.
• [47]. Sonneborn, T.M. (1970). Methods in Paramecium research. In E.D.M. Prescott (Ed.), Methods in cell biology (pp. 241-339). New York, Acad. Press.
• [48]. Sonoike, K., Hihara, Y. & Ikeuchi, M. (2001). Physiological significance of the regulation of photosystem stoichiometry upon high light acclimation of Synechocystis sp. PCC 6803. Plant Cell Physiol. 42: 379-84.
• [49]. Stefanov, D., Petkova, V. & Denev, I.D. (2011). Screening for heat tolerance in common bean (Phaseolus vulgaris L.) lines and cultivars using JIP-test. Sci. Hortic. 128: 1-6.
• [50]. Strasser, B.J. & Strasser, R.J. (1995). Measuring fast fluorescence transients to address environmental questions: the JIP-test. In P. Mathis (Ed.), Photosynthesis: From Light to Biosphere (pp. 977-980). Dordrecht, Kluwer Academic Publishers.
• [51]. Summerer, M., Sonntag, B., Hörtnagl, P. & Sommaruga, R. (2009). Symbiotic ciliates receive protection against UV damage from their algae: A test with Paramecium bursaria and Chlorella. Protist 60(2): 233-243.
• [52]. Teoh, M.L., Phang, S.M. & Chu, W.L. (2013). Response of Antarctic, temperate and tropical microalgae to temperature stress. J. Appl. Phycol. 25: 285-297.
• [53]. Thompson, P.A., Guo, M.X. & Harrison, P.J. (1992). Effects of variation in temperature. I. On the biochemical composition of eight species of marine phytoplankton. J. Phycol. 28: 481-488.
• [54]. Torzillo, G., Bernardini, P. & Masojídek, J. (1998). On-line monitoring of chlorophyll fluorescence to assess the extent of photoinhibition of photosynthesis induced by high oxygen concentration and low temperature and its effect on the productivity of outdoor cultures of Spirulina platensis (cyanobacteria). J. Phycol. 34: 504-510.
• [55]. Vass, I., Styring, S., Hundal, T., Koivuniemi, A., Aro, E. et al. (1992). Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation. Proc. Natl. Acad. Sci. USA 89: 1408-1412.
• [56]. Vonshak, A. & Novoplansky, N. (2008). Acclimation to low temperature of two Arthrospira platensis (cyanobacteria) strains involves down-regulation of PSII and improved resistance to photoinhibition. J. Phycol. 44: 1071-1079.
• [57]. Walters, R.G. & Horton, P. (1995). Acclimation of Arabidopsis thaliana to the light environment: regulation of chloroplast composition. Planta 197: 475-481.
• [58]. Wen, X., Gong, H. & Lu, C. (2005). Heat stress induces an inhibition of excitation energy transfer from phycobilisomes to photosystem II but not to photosystem I in a cyanobacterium Spirulina platensis. Plant Physiol. Bioch. 43: 389-395.
• [59]. Wilson, K.E. & Huner, N.P.A. (2000). The role of growth rate, redox-state of the plastoquinone pool and the transthylakoid DpH in photoacclimation of Chlorella vulgaris to growth irradiance and temperature. Planta 212: 93-102.
• [60]. Wilson, K.E., Król, M. & Huner, N.P.A. (2003). Temperature-induced greening of Chlorella vulgaris. The role of the cellular energy balance and zeaxanthin-dependent nonphotochemical quenching. Planta 217: 616-627.
• [61]. Xu, H., Liu, G., Liu, G., Yan, B., Duan, W. et al. (2014). Comparison of investigation methods of heat injury in grapevine (Vitis) and assessment to heat tolerance in different cultivars and species. BMC Plant Biol. 14: 156-176.
• [62]. Yamada, T., Onimatsu, H. & van Etten, J.L. (2006). Chlorella viruses. Adv. Virus. Res. 66: 293-336.
• [63]. Zhang, M., Yu, Y., Yang, Z. & Kong, F. (2012). Photochemical responses of phytoplankton to rapid increasing-temperature process. Phycol. Res. 60: 199-207.

Uwagi

Opracowanie rekordu w ramach umowy 509/P-DUN/2018 ze środków MNiSW przeznaczonych na działalność upowszechniającą naukę (2018).