Effects of elevated pCO_2 on physiological performance of marine microalgae Dunaliella salina(Chlorophyta, Chlorophyceae)
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摘要
The present study was conducted to determine the ef fects of elevated pCO_2 on growth, photosynthesis, dark respiration and inorganic carbon acquisition in the marine microalga D unaliella salina. To accomplish this, D. salina was incubated in semi-continuous cultures under present-day CO_2 levels(390 μatm, p HN BS : 8.10), predicted year 2100 CO_2 levels(1 000 μatm, p HN BS : 7.78) and predicted year 2300 CO_2 levels(2 000 μatm, p H NBS : 7.49). Elevated pCO_2 significantly enhanced photosynthesis(in terms of gross photosynthetic O_2 evolution, ef fective quantum yield(ΔF/F' m), photosynthetic efficiency( α), maximum relative electron transport rate(r ETRm ax) and ribulose-1,5-bisphosphate carboxylase/oxygenase(Rubisco) activity) and dark respiration of D. salina, but had insignificant effects on growth. The photosynthetic O_2 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 HCO ˉ 3 via extracellular carbonic anhydrase and anion-exchange proteins. Furthermore, the lower inhibition of the photosynthetic O2 evolution at high pCO_2 levels by AZ, EZ and DIDS and the decreased carbonic anhydrase showed that carbon concentrating mechanisms were down-regulated at high pCO_2. In conclusion, our results show that photosynthesis, dark respiration and CCMs will be af fected by the increased pCO_2/low p H conditions predicted for the future, but that the responses of D. salina to high pCO_2/low p H might be modulated by other environmental factors such as light, nutrients and temperature. Therefore, further studies are needed to determine the interactive eff ects of pCO_2, temperature, light and nutrients on marine microalgae.
The present study was conducted to determine the ef fects of elevated pCO_2 on growth, photosynthesis, dark respiration and inorganic carbon acquisition in the marine microalga D unaliella salina. To accomplish this, D. salina was incubated in semi-continuous cultures under present-day CO_2 levels(390 μatm, p HN BS : 8.10), predicted year 2100 CO_2 levels(1 000 μatm, p HN BS : 7.78) and predicted year 2300 CO_2 levels(2 000 μatm, p H NBS : 7.49). Elevated pCO_2 significantly enhanced photosynthesis(in terms of gross photosynthetic O_2 evolution, ef fective quantum yield(ΔF/F' m), photosynthetic efficiency( α), maximum relative electron transport rate(r ETRm ax) and ribulose-1,5-bisphosphate carboxylase/oxygenase(Rubisco) activity) and dark respiration of D. salina, but had insignificant effects on growth. The photosynthetic O_2 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 HCO ˉ 3 via extracellular carbonic anhydrase and anion-exchange proteins. Furthermore, the lower inhibition of the photosynthetic O2 evolution at high pCO_2 levels by AZ, EZ and DIDS and the decreased carbonic anhydrase showed that carbon concentrating mechanisms were down-regulated at high pCO_2. In conclusion, our results show that photosynthesis, dark respiration and CCMs will be af fected by the increased pCO_2/low p H conditions predicted for the future, but that the responses of D. salina to high pCO_2/low p H might be modulated by other environmental factors such as light, nutrients and temperature. Therefore, further studies are needed to determine the interactive eff ects of pCO_2, temperature, light and nutrients on marine microalgae.
The present study was conducted to determine the ef fects of elevated pCO_2 on growth, photosynthesis, dark respiration and inorganic carbon acquisition in the marine microalga D unaliella salina. To accomplish this, D. salina was incubated in semi-continuous cultures under present-day CO_2 levels(390 μatm, p HN BS : 8.10), predicted year 2100 CO_2 levels(1 000 μatm, p HN BS : 7.78) and predicted year 2300 CO_2 levels(2 000 μatm, p H NBS : 7.49). Elevated pCO_2 significantly enhanced photosynthesis(in terms of gross photosynthetic O_2 evolution, ef fective quantum yield(ΔF/F' m), photosynthetic efficiency( α), maximum relative electron transport rate(r ETRm ax) and ribulose-1,5-bisphosphate carboxylase/oxygenase(Rubisco) activity) and dark respiration of D. salina, but had insignificant effects on growth. The photosynthetic O_2 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 HCO ˉ 3 via extracellular carbonic anhydrase and anion-exchange proteins. Furthermore, the lower inhibition of the photosynthetic O2 evolution at high pCO_2 levels by AZ, EZ and DIDS and the decreased carbonic anhydrase showed that carbon concentrating mechanisms were down-regulated at high pCO_2. In conclusion, our results show that photosynthesis, dark respiration and CCMs will be af fected by the increased pCO_2/low p H conditions predicted for the future, but that the responses of D. salina to high pCO_2/low p H might be modulated by other environmental factors such as light, nutrients and temperature. Therefore, further studies are needed to determine the interactive eff ects of pCO_2, temperature, light and nutrients on marine microalgae.
引文
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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.CO 2 and HCO 3 uptake in marine diatoms acclimated to different CO 2 concentrations.Limnol.Oceanogr.,46(6):1 378-1 391.
Caldeira K,Wickett M E.2003.Oceanography:anthropogenic carbon and ocean p H.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 CO 2 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 DA.2008.A comparison of future increased CO 2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum.Harmful Algae,7(1):76-90.
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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
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Heimann S,Schreiber U.1999.Cyt b-559(Fd)participating in cyclic electron transport in spinach chloroplasts:evidence for kinetic connection with the cyt b 6/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.
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Ihnken S,Roberts S,Beardall J.2011.Differential responses of growth and photosynthesis in the marine diatom Chaetoceros muelleri to CO 2 and light availability.Phycologia,50(2):182-193.
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I?íguez C,Lorenzo M R,Niell F X,Wiencke C,Gordillo F J,Carmona Fernández R.2015.Effects of increased CO 2 in the carbon budget and the photosynthetic yield of the arctic seaweeds Alaria esculenta and Desmarestia aculeata.http://hdl.handle.net/10630/9265.
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 p CO 2 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 p CO 2 on early development in the mussel Mytilus galloprovincialis.Aquat.Biol.,4(3):225-233.
Langer G,Geisen M,Baumann K H,Kl?s 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.
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Liu Y T,Xu J T,Gao K S.2012.CO 2-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 CO 2 and bicarbonate transport in the green alga chlorella ellipsoidea(II.Evidence for induction in response to external CO 2concentration).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 CO 2 on photosynthesis and cell components of the red alga Porphyra leucosticta.J.Appl.Phycol.,11(5):455-461.
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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 CO 2 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.
Olischl?ger 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.
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Riebesell U,Schulz K G,Bellerby R G J,Botros M,Fritsche P,Meyerh?fer M,Neill C,Nondal G,Oschlies A,Wohlers J,Z?llner E.2007.Enhanced biological carbon consumption in a high CO 2 ocean.Nature,450(7169):545-548.
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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,Olischl?ger M,Gutow L,Wiencke C.2013.Combined effects of CO 2,temperature,irradiance and time on the physiological performance of Chondrus crispus(Rhodophyta).Bot.Mar.,56(1):63-74.
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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 p H-induced 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 p CO 2 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.PLo SOne,8(6):e65987.
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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.CO 2 and HCO 3 uptake in marine diatoms acclimated to different CO 2 concentrations.Limnol.Oceanogr.,46(6):1 378-1 391.
Caldeira K,Wickett M E.2003.Oceanography:anthropogenic carbon and ocean p H.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 CO 2 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 DA.2008.A comparison of future increased CO 2 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,H?der D P,Li W,Xu K,Liu N N,Riebesell U.2012.Rising CO 2 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.CO 2 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 Heds.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 b 6/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.CO 2 control of Trichodesmium N 2 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 CO 2 and light availability.Phycologia,50(2):182-193.
I?iguez C,Carmona R,Lorenzo M R,Niell F X,Wiencke C,Gordillo F J L.2016.Increased CO 2 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.
I?íguez C,Lorenzo M R,Niell F X,Wiencke C,Gordillo F J,Carmona Fernández R.2015.Effects of increased CO 2 in the carbon budget and the photosynthetic yield of the arctic seaweeds Alaria esculenta and Desmarestia aculeata.http://hdl.handle.net/10630/9265.
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 p CO 2 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 p CO 2 on early development in the mussel Mytilus galloprovincialis.Aquat.Biol.,4(3):225-233.
Langer G,Geisen M,Baumann K H,Kl?s 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 CO 2 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.CO 2-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 CO 2 and bicarbonate transport in the green alga chlorella ellipsoidea(II.Evidence for induction in response to external CO 2concentration).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 CO 2 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 HCO 3ˉuse by the inorganic carbon level in 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 CO 2 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.
Olischl?ger 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,Meyerh?fer M,Neill C,Nondal G,Oschlies A,Wohlers J,Z?llner E.2007.Enhanced biological carbon consumption in a high CO 2 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,Olischl?ger M,Gutow L,Wiencke C.2013.Combined effects of CO 2,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,WulffA.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 p H-induced changes in seawater carbonate chemistry.Physiol Plant,133(1):92-105.
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