Abstract
Arthrospira (Spirulina) is widely used as human health food and animal feed. In cultures grown outdoors in open ponds, Arthrospira cells are subjected to various environmental stresses, such as high temperature. A better understanding of the effects of high temperature on photosynthesis may help optimize the productivity of Arthrospira cultures. In this study, the effects of heat stress on photosynthetic rate, chlorophyll a fluorescence transients, and photosystem (PS) II, PSI activities in a marine cyanobacterium Arthrospira sp. were examined. Arthrospira cells grown at 25 °C were treated for 30 min at 25 (control), 30, 34, 37, or 40 °C in the dark. Heat stress (30–37 °C) enhanced net photosynthetic O2 evolution rate. Heat stress caused over-reduction PSII acceptor side, damage of donor side of PSII, decrease in the energetic connectivity of PSII units, and decrease in the performance of PSII. When the temperature changed from 25 to 37 °C, PSII activity decreased, while PSI activity increased, the enhancement of photosynthetic O2 evolution was synchronized with the increase in PSI activity. When temperature was further increased to 40 °C, it induced a decrease in photosynthetic O2 evolution rate and a more severe decrease in PSII activity, but an increase in PSI activity. These results suggest that PSI activity was the decisive factor determining the change of photosynthetic O2 evolution when Arthrospira was exposed to a temperature from 25 to 37 °C, but then, PSII activity became the decisive factor adjusting the change of photosynthetic O2 evolution when the temperature was increased to 40 °C.
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References
Baker NR (1991) A possible role for photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81:563–570
Bennet J, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58:419–435
Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543
Colla LM, Reinehr CO, Reichert C, Costa JAV (2007) Production of biomass and nutraceutical compounds by Spirulina platensis under different temperature and nitrogen regimes. Bioresour Technol 98:1489–1493
Havaux M (1993) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Sci 94:19–33
Havaux M (1996) Short-term responses of photosystem I to heat stress: induction of a PS II-independent electron transport through PS I fed by stromal components. Photosynth Res 47:85–97
Havaux M, Greppin H, Strasser RJ (1991) Functioning of photosystem I and II in pea leaves exposed to heat stress in the presence or absence of light. Planta 186:88–98
Kalachanis D, Manetas Y (2010) Analysis of fast chlorophyll fluorescence rise (O-K-J-I-P) curves in green fruits indicates electron flow limitations at the donor side of PSII and the acceptor sides of both photosystems. Physiol Plant 139:313–323
Lu C, Vonshak A (1999a) Photoinhibition in outdoor Spirulina platensis cultures assessed by polyphasic chlorophyll fluorescence transients. J Appl Phycol 11:355–359
Lu C, Vonshak A (1999b) Characterization of PSII photochemistry in salt-adapted cells of cyanobacterium Spirulina platensis. New Phytol 141:231–239
Lu C, Zhang J, Vonshak A (1998) Inhibition of quantum yield of PSII electron transport in Spirulina platensis by osmotic stress may be explained mainly by an increase in the proportion of the QB-non-reducing PSII reaction centers. Aust J Plant Physiol 25:689–694
Ogbonda KH, Aminigo RE, Abu GO (2007) Influence of temperature and pH on biomass production and protein biosynthesis in a putative Spirulina sp. Bioresour Technol 98:2207–2211
Pang T, Liu JG, LiuQ ZLT, Lin W (2012) Impacts of glyphosate on photosynthetic behaviors in Kappaphycus alvarezii and Neosiphonia savatieri detected by JIP-test. J Appl Phycol 24:467–473
Qiu NW, Lu CM (2003) Enhanced tolerance of photosynthesis against high temperature damage in salt-adapted halophyte Atriplex centralasiatica plants. Plant Cell Environ 26:1137–1145
Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP test. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer, Dordrecht, pp 977–980
Strasser RJ, Srivatava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor and Francis, London, pp 445–483
Strasser RJ, Tsimill-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Kluwer, Dordrecht, pp 321–362
Torzillo G, Sacchi A, Materassi R, Richmond A (1991) Effect of temperature on yield and night biomass loss in Spirulina platensis grown outdoors in tubular photobioreactors. J Appl Phycol 3:103–109
Tóth SZ, Schansker G, Kissimon J, Kovács L, Garab G, Strasser RJ (2005) Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.). J Plant Physiol 162:181–194
Vonshak A (1997) Use of Spirulina biomass. In: Vonshak A (ed) Spirulina platensis (Arthrospira): physiology, cell-biology and biochemistry. Taylor & Francis, London, pp 205–212
Vonshak A, Abeliovich A, Boussiba S, Richmond A (1982) Production of Spirulina biomass: effect of environmental factors and population density. Biomass 2:175–185
Wen XG, Qiu NW, Lu QT, Lu CM (2005a) Enhanced thermotolerance of photosystem II in salt adapted halophyte Artemisia anethifolia plants. Planta 220:486–497
Wen XG, Gong HM, Lu CM (2005b) Heat stress induces a reversible inhibition of electron transport at the acceptor side of photosystem II in a cyanobacterium Spirulina platensis. Plant Sci 168:1471–1476
Yamane Y, Kashino Y, Koike H, Satoh K (1998) Effects of high temperature on the photosynthetic systems in spinach oxygen-evolving activities, fluorescence characteristics and the denaturation process. Photosynth Res 57:51–59
Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee SNB (2010) Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta 1797:1428–1438
Zarrouk C (1966) Contribution à l'étude d'une cyanophycée: influence de divers facteurs physiques et chimiques sur la croissance et la photosynthèse de Spirulina maxima (Setch et Gardner) Geitler. Thèse de doctorat, Faculté des Sciences de l'Université de Paris
Zhang T, Gong HM, Wen XG, Lu CM (2010) Salt stress induces a decrease in excitation energy transfer from phycobilisomes to photosystem II but an increase to photosystem I in the cyanobacterium Spirulina platensis. J Plant Physiol 167:951–958
Zhang LT, Zhang ZS, Gao HY, Xue ZC, Yang C, Meng XL, Meng QW (2011) Mitochondrial alternative oxdiase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiol Plant 143:396–407
Zhang LT, Gao HY, Zhang ZS, Xue ZC, Meng QW (2012a) Multiple effects of inhibition of mitochondrial alternative oxidase pathway on photosynthetic apparatus in Rumex K-1 leaves. Biol Plantarum 56:365–368
Zhang LT, Zhang ZS, Gao HY, Meng XL, Yang C, Liu JG, Meng XL (2012b) The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biol 12:40
Zhang LT, He ML, Liu JG (2014) The enhancement mechanism of hydrogen photoproduction in Chlorella protothecoides under nitrogen limitation and sulfur deprivation. Int J Hydrogen Energy 39:8969–8976
Zhao BB, Wang J, Gong HM, Wen XG, Ren HY, Lu CM (2008) Effects of heat stress on PSII photochemistry in a cyanobacterium Spirulina platensis. Plant Sci 175:556–564
Acknowledgments
The work was supported by the Key Project of Jiangsu Natural Science Foundation (BK2011009), Prospective Project for Production and Research Cooperation of Jiangsu (BY2013044), and the Innovation Fund Designated for Post Doctors of Shandong Province (201203107).
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Zhang, L., Liu, J. Effects of heat stress on photosynthetic electron transport in a marine cyanobacterium Arthrospira sp.. J Appl Phycol 28, 757–763 (2016). https://doi.org/10.1007/s10811-015-0615-4
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DOI: https://doi.org/10.1007/s10811-015-0615-4