Abstract
Under ocean acidification (OA), the 200 % increase in CO2(aq) and the reduction of pH by 0.3–0.4 units are predicted to affect the carbon physiology and growth of macroalgae. Here we examined how the physiology of the giant kelp Macrocystis pyrifera is affected by elevated pCO2/low pH. Growth and photosynthetic rates, external and internal carbonic anhydrase (CA) activity, HCO3 − versus CO2 use were determined over a 7-day incubation at ambient pCO2 400 µatm/pH 8.00 and a future OA treatment of pCO2 1200 µatm/pH 7.59. Neither the photosynthetic nor growth rates were changed by elevated CO2 supply in the OA treatment. These results were explained by the greater use of HCO3 − compared to CO2 as an inorganic carbon (Ci) source to support photosynthesis. Macrocystis is a mixed HCO3 − and CO2 user that exhibits two effective mechanisms for HCO3 − utilization; as predicted for species that possess carbon-concentrating mechanisms (CCMs), photosynthesis was not substantially affected by elevated pCO2. The internal CA activity was also unaffected by OA, and it remained high and active throughout the experiment; this suggests that HCO3 − uptake via an anion exchange protein was not affected by OA. Our results suggest that photosynthetic Ci uptake and growth of Macrocystis will not be affected by elevated pCO2/low pH predicted for the future, but the combined effects with other environmental factors like temperature and nutrient availability could change the physiological response of Macrocystis to OA. Therefore, further studies will be important to elucidate how this species might respond to the global environmental change predicted for the ocean.
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References
Andría JR, Pérez-Llorens JL, Vergara JJ (1999) Mechanisms of inorganic carbon acquisition in Gracilaria gaditana nom. prov. (Rhodophyta). Planta 208:564–573
Axelsson L, Ryberg H, Beer S (1995) Two models of bicarbonate utilization in the marine green macroalga Ulva lactuca. Plant, Cell Environ 18:439–445
Axelsson L, Larsson C, Ryberg H (1999) Affinity, capacity and oxygen sensitivity of two different mechanisms for bicarbonate utilization in Ulva lactuca L. (Chlorophyta). Plant, Cell Environ 22:969–978
Axelsson L, Mercado JM, Figueroa FL (2000) Utilization of HCO3 − at high pH by the brown macroalga Laminaria saccharina. Eur J Phycol 35:53–59
Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and co–evolution of RUBISCO, plastids, pyrenoids and chloroplast-based CO2 concentrating mechanisms in the algae. Can J Bot 76:1052–1071
Beardall J, Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms and their regulation. Funct Plant Biol 29:335–347
Beardall J, Beer S, Raven JA (1998) Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Bot Mar 41:113–123
Beardall J, Roberts S, Raven JA (2005) Regulation of inorganic carbon acquisition by phosphorus limitation in the green alga Chlorella emersonii. Can J Bot 83:859–864
Beer S (1994) Mechanisms of inorganic carbon acquisition in marine macroalgae (with special reference to the Chlorophyta). Progr Phycol Res 10:179–207
Beer S, Björk M, Beardall J (2014) Photosynthesis in the marine environment. Wiley-Blackwell, Iowa
Bensoussan N, Gattuso JP (2007) Community primary production and calcification in a NW Mediterranean ecosystem dominated by calcareous macroalgae. Mar Ecol Prog Ser 334:37–45
Björk M, Haglund K, Ramazanov Z, Pedersén M (1993) Inducible mechanisms for HCO3 − utilization and repression of photorespiration in protoplasts and thalli of three species of Ulva (Chlorophyta). J Phycol 29:166–173
Brown MB, Edwards MS, Kim KY (2014) Effects of climate change on the physiology of giant kelp, Macrocystis pyrifera, and grazing by purple urchin, Strongylocentrotus purpuratus. Algae 29(3):203–215
Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365
Charpy-Roubaud C, Sournia A (1990) The comparative estimation of phytoplanktonic, microphytobenthic and macrophytobenthic primary production in the oceans. Mar Microb Food Webs 4(1):31–57
Cornwall CE, Hepburn CD, McGraw CM, Currie KI, Pilditch CA, Hunter KA, Boyd PW, Hurd CL (2013) Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc R Soc B 280:20132201
Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements, vol 3. PICES Special Publication, pp 1–191
Drechsler Z, Sharkia R, Cabantchik ZI, Beer S (1993) Bicarbonate uptake in the marine macroalga Ulva sp. is inhibited by classical probes of anion exchange by red blood cells. Planta 191:34–40
Fernández PA, Hurd CL, Roleda MY (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. J Phycol 50:998–1008
Garcia H, Gordon L (1992) Oxygen solubility in seawater: better fitting equations. Limnol Oceanogr 37:1307–1312
García-Sánchez MJ, Fernández JA, Niell X (1994) Effect of inorganic carbon supply on the photosynthetic physiology of Gracilaria tenuistipitata. Planta 194:55–61
Gattuso JP, Gao K, Lee K, Rost B, Schulz KG (2010) Approaches and tools to manipulate the carbonate chemistry. In: Riebesell U, Fabry VJ, Hansson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg, pp 41–51
Geib K, Golldack D, Gimmler H (1996) Is there a requirement for an external carbonic anhydrase in the extremely acid- resistant green alga Dunaliella acidophila? Eur J Phycol 31:273–284
Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131
Gordillo FJ, Niell FX, Figueroa FL (2001) Non–photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213:64–70
Graham M, Vásquez J, Buschmann A (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanogr Mar Biol Annu Rev 45:39–88
Guinotte JM, Fabry VJ (2008) Ocean acidification and its potential effects on marine ecosystems. Ann NY Acad Sci 1134:320–342
Gutow L, Rahman MM, Bartl K, Saborowski R, Bartsch I, Wiencke C (2014) Ocean acidification affects growth, but not nutritional quality of the seaweed Fucus vesiculosus (Phaeophyceae, Fucales). J Exp Mar Biol Ecol 453:84–90
Haglund K, Björk M, Ramazanov Z, Garcia-Reina G, Pedersén M (1992) Role of carbonic anhydrase in photosynthesis and inorganic–carbon assimilation in the red alga Gracilaria tenuistipitata. Planta 187:275–281
Hay CH (1990) The distribution of Macrocystis (Phaeophyta, Laminariales) as a biological indicator of cool sea surface temperature, with special reference to New Zealand waters. J R Soc NZ 20:313–336
Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Change Biol 17:2488–2497
Hunter KA (2007) SWCO2. http://neon.otago.ac.nz/research/mfc/people/keith_hunter/software/swco2. Accessed 5 Oct 2011
Huovinen P, Gómez I, Orostegui M (2007) Patterns and UV sensitivity of carbon anhydrase and nitrate reductase activities in south Pacific macroalgae. Mar Biol 151:1813–1821
Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. J Phycol 45:1236–1251
Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology. Cambridge University Press, Cambridge
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 50:182–193
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 PM (eds) Contribution of working group I to the fifth assessment report (AR5) of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 1535
Israel A, Hophy M (2002) Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations. Glob Change Biol 8:831–840
Kawamitsu Y, Boyer JS (1999) Photosynthesis and carbon storage between tides in a brown alga, Fucus vesiculosus. Mar Biol 133:361–369
Kübler JE, Johnston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant, Cell Environ 22:1303–1310
Leal PP, Hurd CL, Roleda MY (2014) Meiospores produced in sori of nonsporophyllous laminae of Macrocystis pyrifera (Laminariales, Phaeophyceae) may enhance reproductive output. J Phycol 50:400–405
Longphuirt SN, Eschmann C, Russell C, Stengel DB (2013) Seasonal and species–specific response of five brown macroalgae to high atmospheric CO2. Mar Ecol Prog Ser 493:91–102
Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26(3):439–449
Madsen TV, Maberly SC (2003) High internal resistance to CO2 uptake by submerged macrophytes that use HCO3 −: measurements in air, nitrogen and helium. Photosynth Res 77:183–190
Magnusson G, Larsson C, Axelsson L (1996) Effects of high CO2 treatment on nitrate and ammonium uptake by Ulva lactuca grown in different nutrient regimes. Sci Mar 60:179–189
McGraw CM, Cornwall CE, Reid MR, Currie KI, Hepburn CD, Hurd CL, Hunter KA (2010) An automated pH–controlled culture system for laboratory–based ocean acidification experiments. Limnol Oceanogr Methods 8:686–694
Mercado JM, Niell FX, Figueroa FL (1997) Regulation of the mechanism for HCO3 − use by the inorganic carbon level in Porphyra leucosticta Thur. in Le Jolis (Rhodophyta). Planta 201:319–325
Mercado JM, Javier F, Gordillo L, Niell FX, Figueroa FL (1999) Effects of different levels of CO2 on photosynthesis and cell components of the red alga Porphyra leucosticta. J Apply Phycol 11:455–461
Mercado JM, Andría JR, Pérez-Llorens JL, Vergara JJ, Axelsson L (2006) Evidence for a plasmalemma–based CO2 concentrating mechanism in Laminaria saccharina. Photosynth Res 88:259–268
Millero F, Poisson A (1981) International one–atmosphere equation of state of seawater. Deep-Sea Res 28A:625–629
Moroney JV, Husic HD, Tolbert NE (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79:177–183
Pérez-Lloréns JL, Brun FG, Andría J, Vergara JJ (2004) Seasonal and tidal variability of environmental carbon related physico–chemical variables and inorganic C acquisition in Gracilariopsis longissima and Enteromorpha intestinalis from Los Torunos salt marsh (Cádiz Bay, Spain). J Exp Mar Biol Ecol 304:183–201
Rautenberger R, Fernández PA, Strittmatter M, Heesch S, Cornwall CE, Hurd CL, Roleda MY (2015) Saturating light and not increased carbon dioxide under ocean acidification drives photosynthesis and growth in Ulva rigida (Chlorophyta). Ecol Evol 5(4):874–888
Raven JA (1991) Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: relation to increased CO2 and temperature. Plant, Cell Environ 14:779–794
Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27:85–209
Raven JA, Hurd CL (2012) Ecophysiology of photosynthesis in macroalgae. Photosynth Res 113:105–125
Roleda MY, Hurd CL (2012) Seaweeds responses to ocean acidification. In: Wiencke C, Bischof K (eds) Seaweed biology, ecological studies 219. Springer-Verlag, Berlin, pp 407–431
Roleda MY, Morris JN, McGraw CM, Hurd CL (2012) Ocean acidification and seaweed reproduction: increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Glob Change Biol 18(3):854–864
Rothäusler E, Gómez I, Hinojosa IA, Karsten U, Tala F, Thiel M (2011) Physiological performance of floating giant kelp Macrocystis pyrifera (Phaeophyceae): Latitudinal variability in the effects of temperature and grazing. J Phycol 47:269–281
Suárez-Álvarez S, Gómez-Pinchetti JL, García-Reina G (2011) Effects of increased CO2 levels on growth, photosynthesis, ammonium uptake and cell composition in the macroalga Hypnea spinella (Gigartinales, Rhodophyta). J Apply Phycol 24(4):815–823
Swanson AK, Fox CH (2007) Altered kelp (Laminariales) phlorotannins and growth under elevated carbon dioxide and ultraviolet–B treatments can influence associated intertidal food webs. Glob Change Biol 13:1696–1709
The Royal Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy document 12/05 Royal Society, London. The Clyvedon Press Ltd, Cardiff
Thom RM (1996) CO2–enrichment effects on eelgrass (Zostera marina L.) and bull kelp (Nereocystis luetkeana (Mert.) P.&R.). Water Air Soil Poll 88:383–391
Xu Z, Gao K (2009) Impacts of UV radiation on growth and photosynthetic carbon acquisition in Gracilaria lemaneiformis (Rhodophyta) under phosphorus–limited and replete conditions. Funct Plant Biol 36:1057–1064
Sarker MY, 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 56:63–74
Zou D (2005) Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250:726–735
Zou DH, Gao KS (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48:510–517
Zou D, Gao K, Xia J (2003) Photosynthetic utilization of inorganic carbon in the economic brown alga, Hizikia fusiforme (Sargassaceae) from the south china sea. J Phycol 39:1095–1100
Zou D, Gao K, Luo H (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 47:87–97
Acknowledgments
We acknowledge the support of a PhD scholarship from the Chilean government to Pamela A. Fernández (BECAS CHILE-CONICYT) and a grant from The Royal Society of New Zealand Marsden fund (UOO0914) to Catriona L. Hurd. The authors are grateful to Pablo Leal for his help with seaweed collection.
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Fernández, P.A., Roleda, M.Y. & Hurd, C.L. Effects of ocean acidification on the photosynthetic performance, carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera . Photosynth Res 124, 293–304 (2015). https://doi.org/10.1007/s11120-015-0138-5
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DOI: https://doi.org/10.1007/s11120-015-0138-5