Cite this paper:
HU Shunxin, WANG You, WANG Ying, ZHAO Yan, ZHANG Xinxin, ZHANG Yongsheng, JIANG Ming, TANG Xuexi. Effects of elevated pCO2 on physiological performance of marine microalgae Dunaliella salina (Chlorophyta, Chlorophyceae)[J]. HaiyangYuHuZhao, 2018, 36(2): 317-328

Effects of elevated pCO2 on physiological performance of marine microalgae Dunaliella salina (Chlorophyta, Chlorophyceae)

HU Shunxin1, WANG You1, WANG Ying1, ZHAO Yan1, ZHANG Xinxin1, ZHANG Yongsheng1,2, JIANG Ming1, TANG Xuexi1
1 College of Marine Life Science, Ocean University of China, Qingdao 266003, China;
2 Rongcheng Ocean and Fisheries Bureau, Weihai 264300, China
The present study was conducted to determine the effects of elevated pCO2 on growth, photosynthesis, dark respiration and inorganic carbon acquisition in the marine microalga Dunaliella salina. To accomplish this, D. salina was incubated in semi-continuous cultures under present-day CO2 levels (390 μatm, pHNBS:8.10), predicted year 2100 CO2 levels (1 000 μatm, pHNBS:7.78) and predicted year 2300 CO2 levels (2 000 μatm, pHNBS:7.49). Elevated pCO2 significantly enhanced photosynthesis (in terms of gross photosynthetic O2 evolution, effective quantum yield (△F/F'm), photosynthetic efficiency (α), maximum relative electron transport rate (rETRmax) and ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity) and dark respiration of D. salina, but had insignificant effects on growth. The photosynthetic O2 evolution of D. salina was significantly inhibited by the inhibitors acetazolamide (AZ), ethoxyzolamide (EZ) and 4,4'-diisothiocyanostilbene-2,2'-disulfonate (DIDS), indicating that D. salina is capable of acquiring HCO3- via extracellular carbonic anhydrase and anion-exchange pr 3 oteins. Furthermore, the lower inhibition of the photosynthetic O2 evolution at high pCO2 levels by AZ, EZ and DIDS and the decreased carbonic anhydrase showed that carbon concentrating mechanisms were down-regulated at high pCO2. In conclusion, our results show that photosynthesis, dark respiration and CCMs will be affected by the increased pCO2/low pH conditions predicted for the future, but that the responses of D. salina to high pCO2/low pH might be modulated by other environmental factors such as light, nutrients and temperature. Therefore, further studies are needed to determine the interactive effects of pCO2, temperature, light and nutrients on marine microalgae.
Key words:    ocean acidification|growth|photosynthesis|CO2|CCMs|Dunaliella salina   
Received: 2016-10-08   Revised:
PDF (443 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by HU Shunxin
Articles by WANG You
Articles by WANG Ying
Articles by ZHAO Yan
Articles by ZHANG Xinxin
Articles by ZHANG Yongsheng
Articles by JIANG Ming
Articles by TANG Xuexi
Axelsson L, Ryberg H, Beer S. 1995. Two modes of bicarbonate utilization in the marine green macroalga Ulva lactuca.Plant Cell Environ., 18(4):439-445.
Badger M R, Andrews T J, Whitney S M, et al. 1998. The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can J Bot, 76(6):1 052-1071.
Booth W A, Beardall J. 1991. Effects of salinity on inorganic carbon utilization and carbonic anhydrase activity in the halotolerant alga Dunaliella salina (Chlorophyta).Phycologia, 30(2):220-225.
Burkhardt S, Amoroso G, Riebesell U, Sültemeyer D. 2001.CO2 and HCO3 uptake in marine diatoms acclimated to different CO2 concentrations. Limnol. Oceanogr., 46(6):1 378-1 391.
Caldeira K, Wickett M E. 2003. Oceanography:anthropogenic carbon and ocean pH. Nature, 425(6956):365.
del Giorgio P A, Duarte C M. 2002. Respiration in the open ocean. Nature, 420(6914):379-384.
Eberlein T, van de Waal D B, Brandenburg K M, John U, Voss M, Achterberg E P, Rost B. 2016. Interactive effects of ocean acidification and nitrogen limitation on two bloomforming dinoflagellate species. Mar. Ecol. Prog. Ser., 543:127-140.
Falkowski P G, Raven J A. 2013. Aquatic Photosynthesis. Princeton University Press, Princeton.
Fernández P A, Roleda M Y, Hurd C L. 2015. Effects of ocean acidification on the photosynthetic performance, carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera. Photosynth. Res., 124(3):293-304.
Fu F X, Warner M E, Zhang Y H, Feng Y Y, Hutchins D A. 2007. Effects of increased temperature and CO2 on photosynthesis, growth, and elemental ratios in marine Synechococcus and Prochlorococcus (Cyanobacteria). J.Phycol., 43(3):485-496.
Fu F X, Zhang Y H, Warner M E, Feng Y Y, Sun J, Hutchins D A. 2008. A comparison of future increased CO2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae, 7(1):76-90.
Gao K S, Xu J T, Gao G, Li Y H, Hutchins D A, Huang B Q, Wang L, Zheng Y, Jin P, Cai X N, Häder D P, Li W, Xu K, Liu N N, Riebesell U. 2012. Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nat. Climate Change, 2(7):519-523.
Geider R J, Osborne B A. 1989. Respiration and microalgal growth:a review of the quantitative relationship between dark respiration and growth. New Phytol., 112(3):327-341.
Gerard V A, Driscoll T. 1996. A spectrophotometric assay for rubisco activity:application to the kelp Laminaria saccharina and implications for radiometric assays1. J.Phycol., 32(5):880-884
Giordano M, Beardall J, Raven J A. 2005. CO2 concentrating mechanisms in algae:mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol., 56(1):99-131.
Giordano M, Maberly S C. 1989. Distribution of carbonic anhydrase in British marine macroalgae. Oecologia., 81(4):534-539.
Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In:Smith W L, Chanley M H eds. Culture of Marine Invertebrate Animals. Springer, New York, USA. p.29-60
Guinotte J M, Fabry V J. 2008. Ocean acidification and its potential effects on marine ecosystems. Ann. N. Y. Acad.Sci., 1134(1):320-42.
Heimann S, Schreiber U. 1999. Cyt b-559 (Fd) participating in cyclic electron transport in spinach chloroplasts:evidence for kinetic connection with the cyt b6/f complex. Plant Cell Physiol., 40(8):818-824.
Huertas I E, Lubián L M. 1998. Comparative study of dissolved inorganic carbon utilization and photosynthetic responses in Nannochloris (chlorophyceae) and Nannochloropsis(eustigmatophyceae) species. Can. J. Bot., 76(6):1 104-1 108.
Hutchins D A, Fu F X, Zhang Y, Warner M E, Feng Y, Portune K, Bernhardt P W, Mulholland M R. 2007. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios:Implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr., 52(4):1 293-1 304.
Ihnken S, Roberts S, Beardall J. 2011. Differential responses of growth and photosynthesis in the marine diatom Chaetoceros muelleri to CO2 and light availability.Phycologia, 50(2):182-193.
Iñiguez C, Carmona R, Lorenzo M R, Niell F X, Wiencke C, Gordillo F J L. 2016. Increased CO2 modifies the carbon balance and the photosynthetic yield of two common arctic brown seaweeds:Desmarestia aculeata and Alaria esculenta. Polar Biol., 39(11):1 979-1 991.
Iñíguez C, Lorenzo M R, Niell F X, Wiencke C, Gordillo F J, Carmona Fernández R. 2015. Effects of increased CO2 in the carbon budget and the photosynthetic yield of the arctic seaweeds Alaria esculenta and Desmarestia aculeata.
IPCC. 2013. Climate Change 2013:the physical science basis. In:Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley P M eds.Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change.Cambridge University Press, Cambridge. p.1 535.
Kranz S A, Dieter S, Richter K U, Rost B. 2009. Carbon acquisition by Trichodesmium:the effect of pCO2 and diurnal changes. Limnol. Oceanogr., 54(2):548-559.
Krause G H, Jahns P. 2004. Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching:characterization and function. In:Papageorgiou G C, Govindjee eds. Chlorophyll a Fluorescence. Springer, Netherlands. p.463-495
Kurihara H, Asai T, Kato S, Ishimatsu A. 2008. Effects of elevated pCO2 on early development in the mussel Mytilus galloprovincialis. Aquat. Biol., 4(3):225-233.
Langer G, Geisen M, Baumann K H, Kläs J, Riebesell U, Thoms S, Young J R. 2006. Species-specific responses of calcifying algae to changing seawater carbonate chemistry.Geochem. Geophys. Geosyst., 7(9):535-540.
Lewis E, Wallace D, Allison L J. 1998. Program developed for CO2 system calculations. Tennessee:Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy.
Liu Y T, Xu J T, Gao K S. 2012. CO2-driven seawater acidification increases photochemical stress in a green alga. Phycologia, 51(5):562-566.
Liu Z Y, Zhang L J, Cai W J, Wang L, Xue M, Zhang X S. 2014. Removal of dissolved inorganic carbon in the yellow river estuary. Limnol. Oceanogr., 59(2):413-426.
Matsuda Y, Colman B. 1995. Induction of CO2 and bicarbonate transport in the green alga chlorella ellipsoidea (Ⅱ. Evidence for induction in response to external CO2 concentration). Plant Physiol., 108(1):253-260.
Mercado J M, Javier F, Gordillo L, Niell F X, Figueroa F L. 1999. Effects of different levels of CO2 on photosynthesis and cell components of the red alga Porphyra leucosticta.J. Appl. Phycol., 11(5):455-461.
Mercado J M, Niell F X, Figueroa F L. 1997. Regulation of the mechanism for HCO3- use by the inorganic carbon level in 3 Porphyra leucosticta Thur. in Le Jolis (Rhodophyta).Planta, 201(3):319-325.
Moroney J V, Husic H D, Tolbert N E. 1985. Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol., 79(1):177-183.
Moroney J V, Somanchi A. 1999. How do algae concentrate CO2 to increase the efficiency of photosynthetic carbon fixation?. Plant Physiol., 119(1):9-16.
Nimer N A, Iglesias-Rodriguez M D, Merrett M J. 1997.Bicarbonate utilization by marine phytoplankton species.J. Phycol., 33(4):625-631.
Olischläger M, Wiencke C. 2013. Ocean acidification alleviates low-temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (rhodophyta). J. Exp.Bot., 64(18):5 587-5 597.
Platt T, Gallegos C L, Harrison W G. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res., 38:687-701.
Ralph P J, Gademann R. 2005. Rapid light curves:a powerful tool to assess photosynthetic activity. Aquat. Bot., 82(3):222-237.
Reinfelder J R. 2011. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu. Rev. Mar. Sci., 3(1):291-315.
Riebesell U, Schulz K G, Bellerby R G J, Botros M, Fritsche P, Meyerhöfer M, Neill C, Nondal G, Oschlies A, Wohlers J, Zöllner E. 2007. Enhanced biological carbon consumption in a high CO2 ocean. Nature, 450(7169):545-548.
Rost B, Richter K U, Riebesell U, Hansen P J. 2006. Inorganic carbon acquisition in red tide dinoflagellates. Plant Cell Environ., 29(5):810-822.
Rost B, Riebesell U, Burkhardt S, Sültemeyer D. 2003. Carbon acquisition of bloom-forming marine phytoplankton.Limnol. Oceanogr, 48(1):55-67.
Sarker M Y, Bartsch I, Olischläger M, Gutow L, Wiencke C. 2013. Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus crispus (Rhodophyta). Bot. Mar., 56(1):63-74.
Spreitzer R J, Salvucci M E. 2002. RUBISCO:structure, regulatory interactions, and possibilities for a better enzyme. Annu. Rev. Plant Biol., 53(1):449-475.
Torstensson A, Chierici M, Wulff A. 2012. The influence of increased temperature and carbon dioxide levels on the benthic/sea ice diatom navicula directa. Polar Biol., 35(2):205-214.
Trimborn S, Lundholm N, Thoms S, Richter K U, Krock B, Hansen P J, Rost B. 2008. Inorganic carbon acquisition in potentially toxic and non-toxic diatoms:the effect of pHinduced changes in seawater carbonate chemistry. Physiol Plant, 133(1):92-105.
Trimborn S, Wolf-Gladrow D, Richter K U, Rost B. 2009. The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms. J. Exp. Mar. Biol. Ecol., 376(1):26-36.
Van de Waal D B, John U, Ziveri P, Reichart G J, Hoins M, Sluijs A, Rost B. 2013. Ocean acidification reduces growth and calcification in a marine dinoflagellate. PLoS One, 8(6):e65987.
Wellburn A R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol., 144(3):307-313.
Wu Y P, Beardall J, Gao K S. 2015. Physiological responses of a model marine diatom to fast pH changes:special implications of coastal water acidification. PLoS One, 10(10):e0141163.
Wu Y, Gao K, Riebesell U. 2010. CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences, 7(9):2 915-2 923.
Xu J T, Gao K S. 2012. Future CO2-induced ocean acidification mediates the physiological performance of a green tide alga. Plant Physiol., 160(4):1 762-1 769.
Yang G Y, Gao K S. 2012. Physiological responses of the marine diatom Thalassiosira pseudonana to increased pCO2 and seawater acidity. Mar. Environ. Res., 79:142-151.
Zhang X X, Tang X X, Zhou B, Hu S X, Wang Y. 2015. Effect of enhanced UV-B radiation on photosynthetic characteristics of marine microalgae Dunaliella salina(Chlorophyta, Chlorophyceae). J. Exp. Mar. Biol. Ecol., 469:27-35.
Zou D H, Gao K S, Luo H J. 2011. short-and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (Sargassaceae, Phaeophyta) grown at low and high N supplies. J. Phycol., 47(1):87-97.
Zou D H, Gao K S. 2009. Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia, 48(6):510-517.