Effects of Warming on Carbon Utilization and Photosynthesis of Marine Primary Producers

Main Article Content

Chanida Saewong
Sirinattha Namnapol
Ming Sheng Ng
Sutinee Sinutok
Pimchanok Buapet


Climate warming is among the most important threats to the health of shallow-water marine primary producers. In the present study, heat stress responses were investigated in the seagrass Thalassia hemprichii and the two macroalgae Padina boryana and Ulva intestinalis by comparing dissolved inorganic carbon (DIC) utilization, photosynthesis (as maximum quantum yield [Fv/Fm] and effective quantum yield [φPSII]), and reactive oxygen species (ROS) production after 4 h of exposure to control temperature (30 °C) or warming (40 °C). At 30 °C, DIC uptake rate of U. intestinalis was highest, whereas rates for T. hemprichii and P. boryana were comparable. Warming significantly reduced DIC use in all species. DIC use of U. intestinalis was affected to the greatest extent (from 16.38±0.88 μmol⋅g-1FW⋅h-1 in 30 °C to −1.39±0.36 μmol⋅g-1FW⋅h-1 in 40 °C). Warming significantly reduced the efficiency of photosynthesis in all species. Thalassia hemprichii showed the smallest reduction in Fv/Fm (from 0.80±0.03 in 30 °C to 0.66±0.12 in 40 °C). However, down-regulation of φPSII by warming in all species was comparable (reaching 0.15-0.18). Warming did not increase ROS accumulation in T. hemprichii (45.84±5.32 and 50.30±5.94 fluorescence units at 30 °C and 40 °C, respectively) or P. boryana (48.40±6.27 and 35.60±6.27 fluorescence units at 30 °C and 40 °C, respectively) but decreased accumulation of ROS in U. intestinalis (from 85.31±4.56 fluorescence units at 30 °C to 46.63±12.37 fluorescence units at 40 °C). Leakage of ROS from damaged algal thalli may contribute to the decrease in ROS observed in our study.


Download data is not yet available.

Article Details



Allakhverdiev, S.I., V.D. Kreslavski, V.V. Klimov, D.A. LOS, R. Carpentier and P. Mohanty. 2008. Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis Research 98: 541-550. DOI: 10.1007/s11120-008-9331-0.

Axelsson, L., H. Ryberg and S. Beer. 1995. Two modes of bicarbonate utilization in the marine green macroalgae Ulva lactuca. Plant, Cell and Environment 18: 439-445. DOI: 10.1111/j.1365-3040.1995.tb00378.x.

Berry, J. and O. Björkman. 1980. Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31: 491-543. DOI: 10.1146/annurev.pp.31.060180.002423.

Björk, M., L. Axelsson and S. Beer. 2004. Why is Ulva intestinalis the only macroalga inhabiting isolated rockpools along the Swedish Atlantic coast? Marine Ecology Progress Series 284: 109-116. DOI: 10.3354/meps284109.

Bowes, G. 1991. Growth at elevated CO2: Photosynthetic responses mediated through Rubisco. Plant, Cell and Environment 14(8): 795-806. DOI: 10.1111/j.1365-3040.1991.tb01443.x.

Buapet, P., F. Makkliang, C. Thammakhet-Buranachai. 2017. Photosynthetic activity and photoprotection in green and red leaves of the seagrasses, Halophila ovalis and Cymodocea rotundata: implications for the photoprotective role of anthocyanin. Marine Biology 164: 182. DOI: 10.1007/s00227-017-3215-9.

Buapet, P., M. Gullström and M. Björk. 2013a. Photosynthetic activity of seagrasses and macroalgae in temperate shallow waters can alter seawater pH and total inorganic carbon content at the scale of a coastal embayment. Marine and Freshwater Research 64: 1040-1048. DOI: 10.1071/MF12124.

Buapet, P., M.L. Rasmusson, M. Gullström and M. Björk. 2013b. Photorespiration and Carbon Limitation Determine Productivity in Temperate Seagrasses. PLoS ONE 8(12): e83804. DOI: 10.1371/journal.pone.0083804.

Campbell, S.J., L.J. McKenzie and S.P. Kerville. 2006. Photosynthetic responses of seven tropical seagrasses to elevated seawater temperature. Journal of Experimental Marine Biology and Ecology 330: 455-468. DOI: 10.1016/j.jembe.2005.09.017.

Chan T., Y. Shimizu, P. Pospíšil, N. Nijo, A. Fujiwara, Y. Taninaka, T. Ishikawa, H. Hori, D. Nanba, A. Imai, N. Morita, M. Yoshioka-Nishimura, Y. Izumi, Y. Yamamoto, H. Kobayashi, N. Mizusawa, H. Wada and Y. Yamamoto. 2012. Quality control of photosystem II: lipid peroxidation accelerates photoinhibition under excessive illumination. PLoS ONE 7: e52100. DOI: 10.1371/journal.pone.0052100.

Demmig-Adams, B. 1990. Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1020(1): 1-24. DOI: 10.1016/0005-2728(90)90088-l.

Eggert, A. 2012. Seaweed responses to temperature. In: Seaweed Biology (eds C. Wiencke and K. Bischof), pp. 47-66. Springer-Verlag, Berlin, Germany.

Fang, Y., Z. Jiang, C. Zhao, L. Li, C.I.P.M. Ranvilage, S. Liu, Y. Wu and X. Huang. 2020. Efficient heat dissipation and cyclic electron flow confer daily air exposure tolerance in the intertidal seagrass Halophila beccarii asch. Frontiers in Plant Science 11: 571627. DOI: 10.3389/fpls.2020.571627.

Fernández, P.A., C.L. Hurd and M.Y. Roleda. 2014. Bicarbonate uptake via an anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH. Journal of Phycology 50: 998-1008. DOI: 10.1111/jpy.12247.

George, R., M. Gullström, M.M. Mangora, M.S.P. Mtolera and M. Björk. 2018. High midday temperature stress has stronger effects on biomass than on photosynthesis: A mesocosm experiment on four tropical seagrass species. Ecology and Evolution 8: 4508-4517. DOI: 10.1002/ece3.3952.

Hellblom, F., S. Beer and M. Björk. 2001. A buffer sensitive inorganic carbon utilization system in Zostera marina. Aquatic botany 69: 55-62. DOI: 10.1016/S0304-3770(00)00132-7.

Ilík, P., M. Špundová, M. Šicner, H. Melkovičová, Z. Kučerová, P. Krchňák, T. Fürst, K. Večeřová, K. Panzarová, Z. Benediktyová and M. Trtílek. 2018. Estimating heat tolerance of plants by ion leakage: a new method based on gradual heating. New Phytologist 218(3): 1278-1287. DOI: 10.1111/nph.15097.

Inaba, M. and P. Grandall. 1988. Electrolyte leakage as an indicator of high-temperature injury to harvested mature green tomatoes. Journal of The American Society for Horticultural Science 113: 96-99.

Laffoley, D. and G. Grimsditch. 2009. The Management of Natural Coastal Carbon Sinks. International Union for Conservation of Nature, Gland, Switzerland. 53 pp.

Larsson, C. and L. Axelsson. 1999. Bicarbonate uptake and utilization in marine macroalgae. European Journal of Phycology 34(1): 79-86. DOI: 10.1080/09670269910001736112.

Li, H., H. Xu, P. Zhang, M. Gao, D. Wang and H. Zhao. 2017. High temperature effects on D1 protein turnover in three wheat varieties with different heat susceptibility. Plant Growth Regulation 81: 1-9. DOI: 10.1007/s10725-016-0179-6.

Lilley, R.M.C., P.J. Ralph and A.W.D. Larkum. 2010. The determination of activity of the enzyme Rubisco in cell extractions of the dinoflagellate alga Symbiodinium sp. by manganese chemiluminescence and its response to short-term thermal stress of the alga. Plant, Cell and Environment 33: 995-1004. DOI: 10.1111/j.1365-3040.2010.02121.x.

Manassa, R.P., T.M. Smith, J. Beardall, M. Keough and P.L.M. Cook. 2017. Capacity of a temperate intertidal seagrass species to tolerate changing environmental conditions: significance of light and tidal exposure. Ecological Indicators 81: 578-586. DOI: 10.1016/j.ecolind.2017.04.056.

Marín-Guirao, L., J.M. Ruiz, E. Dattolo, R. Garcia-Munoz and G. Procaccini. 2016. Physiological and molecular evidence of differential short-term heat tolerance in Mediterranean seagrasses. Scientific Reports 6: 28615. DOI: 10.1038/srep28615.

Martone, P.T., M. Alyono and S. Stites. 2010. Bleaching of an intertidal coralline alga: untangling the effects of light, temperature, and desiccation. Marine Ecology Progress Series 416: 57-67.

Pedersen, O., T.D. Colmer, J. Borum, A. Zavala-Perez and G.A. Kendrick. 2016. Heat stress of two tropical seagrass species during low tides - impact on underwater net phot7 osynthesis, dark respiration and diel in situ internal aeration. New Phytologist 210(4): 1207-1218. DOI: 10.1111/nph.13900.

Phandee, S. and P. Buapet. 2018. Photosynthetic and antioxidant responses of the tropical intertidal seagrasses Halophila ovalis and Thalassia hemprichii to moderate and high irradiances. Botanica Marina 61(3): 247-256. DOI: 10.1515/bot-2017-0084.

Rasmusson, L.M., P. Buapet, R. George, M. Gullström, P.C.B. Gunnarsson and M. Björk. 2020. Effects of temperature and hypoxia on respiration, photorespiration, and photosynthesis of seagrass leaves from contrasting temperature regimes. ICES Journal of Marine Science 77(6): 2056-2065. DOI: 10.1093/icesjms/fsaa093.

Raven, J.A. 1997. Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research 27: 85-209. DOI: 10.1016/S0065-2296(08)60281-5.

Resplandy, L., R.F. Keeling, Y. Eddebbar, M.K. Brooks, R. Wang, L. Bopp, M.C. Long, J.P. Dunne, W. Koeve and A. Oschlies. 2018. Quantification of ocean heat uptake from changes in atmospheric O2 and CO2 composition. Nature 563: 105-108. DOI: 10.1038/s41586-018-0651-8.

Riley, J. P. 1975. Analytical chemistry of sea water. In: Chemical Oceanography, 3rd ed. (eds. J.P. Riley and G. Skirrow), pp. 193-514. Academic Press, London, UK.

Roberfroid, M. and P.B. Calderon. 1995. Free Radicals and Oxidation Phenomena in Biological Systems. Dekker, New York, USA. 66 pp.

Roleda, M.Y., P.W. Boyd and C.L. Hurd. 2012a. Before ocean acidification: calcifier chemistry lessons. Journal of Phycology 48: 840-843. DOI: 10.1111/j.1529-8817.2012.01195.x.

Ruelland, E and A. Zachowski. 2010. How plants sense temperature. Environmental and Experimental Botany 69(3): 225-232. DOI: 10.1016/j.envexpbot.2010.05.011.

Salvucci, M.E. and S.J. Crafts-Brandner. 2004. Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiologia Plantarum 120(2): 179-186. DOI: 10.1111/j.0031-9317.2004.0173.x.

Sharma, P., A.B. Jha, R.S. Dubey and M. Pessarakli. 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012: 1-26. DOI: 10.1155/2012/217037.

Smith, S.V. and W.D. Kinsey. 1978. Calcification and organic carbon metabolism as indicated by carbon dioxide. In: Coral Reef: Research Methods (eds. D.R. Stoddart and R.E. Johannes.), pp. 469-484. United Nations Educational, Scientific and Cultural Organization, Paris, France.

Strydom, S., K. Murray, S. Wilson, B. Huntley, M. Rule, M. Heithaus, C. Bessey, G.A. Kendrick, D. Burkholder. M.W. Fraser and K. Zdunic. 2020. Too hot to handle: unprecedented seagrass death driven by marine heatwave in a World Heritage Area. Global Change Biology 26(6): 3525-3538. DOI: 10.1111/gcb.15065.

Van Hees, D. and K. van Alstyne. 2013. Effects of emertion, temperature, dopamine, and hypoxia on extracellular oxidant accumulations surrounding the bloom-forming seaweeds Ulva lactuca and Ulvaria obscura. Journal of Experimental Marine Biology and Ecology 448: 207-213. DOI: 10.1016/j.jembe.2013.07.013.

Viana, I.G., A. Moreira-Saporiti and M. Teichberg. 2020. Species-specific trait responses of three tropical seagrasses to multiple stressors: the case of increasing temperature and nutrient enrichment. Frontiers in Plant Science 11: 571363. DOI: 10.3389/fpls. 2020.571363.

Wei, Z., J. Mo, R. Huang, Q. Hu, C. Long, D. Ding, F. Yang, L. Long. 2020. Physiological performance of three calcifying green macroalgae Halimeda species in response to altered seawater temperatures. Acta Oceanologica Sinica 39: 89-100.

Wuthirak, T., R. Kongnual and P. Buapet. 2016. Desiccation tolerance and underlying mechanisms for the recovery of the photosynthetic efficiency in the tropical intertidal seagrasses Halophila ovalis and Thalassia hemprichii. Botanica Marina 59(5): 387-396. DOI: 10.1515/bot-2016-0052.

Yamamoto, Y. 2016. Quality control of Photosystem II: the mechanisms for avoidance and tolerance of light and heat stresses are closely linked to membrane fluidity of the thylakoids. Frontiers in Plant Science 7: 1136. DOI: 10.3389/fpls.2016.01136.