碳酸酐酶在大型海洋褐藻获取与利用无机碳过程中的作用
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摘要
与大型海洋红藻和绿藻相比,褐藻的生产力最大。碳是构成生物质的主要元素,它在海水中的主要存在形式是HCO_3~–;而HCO_3~–如何进入褐藻细胞而被光合同化为生物质,是人们一直在探讨的问题。综述了迄今为止有关褐藻对无机碳利用的研究结果,指出由碳酸酐酶(carbonic anhydrase, CA)介导的HCO_3~–应是褐藻从海水环境中获取无机碳的主要途径。鉴于微藻细胞内不同细胞器之间存在无机碳转运的事实,褐藻CA在此过程中也起着不可忽视的作用。基于对不同褐藻CA活性的检测结果推测,CA应分布于细胞的不同部位,至少存在于胞内和周质空间中,以应对细胞内外界环境的变化。对不同亚型的CA在褐藻细胞乃至组织中时空分布格局的研究,是探讨褐藻细胞如何获取并高效利用无机碳的关键。
In comparison with red and green macroalgae, brown one has the largest biomass per unit area. Carbon is the main element of biomass. How inorganic carbon enters brown macroalgal cells and consequently is used for fixation by photosynthesis is an open problem that we want to know. Up to date, a large amount of investigations on the utilization of inorganic carbon by brown macroalgae have shown that HCO_3~– mediated by carbonic anhydrase(CA) should be the main way for brown macroalgae to obtain inorganic carbon from marine environment. The fact that inorganic carbon can be interconverted and transported through the organelle membrane in microalgae cells suggested that brown macroalgal CA might play an important role in this process. The detected CA activity in different brown macroalgae suggested that CA should be distributed in different compartments of the cell, at least in the intracellular and periplasmic spaces, thus in response to the intracellular and intercellular changes. At last, it was pointed out that the spatial and temporal distribution pattern of CA in brown macroalgal cells and tissues was the key to explore how to obtain and utilize inorganic carbon efficiently by brown seaweeds.
In comparison with red and green macroalgae, brown one has the largest biomass per unit area. Carbon is the main element of biomass. How inorganic carbon enters brown macroalgal cells and consequently is used for fixation by photosynthesis is an open problem that we want to know. Up to date, a large amount of investigations on the utilization of inorganic carbon by brown macroalgae have shown that HCO_3~– mediated by carbonic anhydrase(CA) should be the main way for brown macroalgae to obtain inorganic carbon from marine environment. The fact that inorganic carbon can be interconverted and transported through the organelle membrane in microalgae cells suggested that brown macroalgal CA might play an important role in this process. The detected CA activity in different brown macroalgae suggested that CA should be distributed in different compartments of the cell, at least in the intracellular and periplasmic spaces, thus in response to the intracellular and intercellular changes. At last, it was pointed out that the spatial and temporal distribution pattern of CA in brown macroalgal cells and tissues was the key to explore how to obtain and utilize inorganic carbon efficiently by brown seaweeds.
引文
[1]Millero FJ.Chemical Oceanography[M].4th Ed.Boca Raton:CRC Press,2013:259-333
[2]Taiz L,Zeiger E.Plant Physiology[M].5th Ed.Sunderland:Sinauer Associates Inc.,2010:67-83
[3]Raven JA.Inorganic carbon acquisition by marine autotrophs.Adv Bot Res,1997,27:85-209
[4]Bartsch I,Wiencke C,Bischof K,et al.The genus Laminaria sensu lato:recent insights and developments.Eur J Phycol,2008,43:1-86
[5]Uehlein N,Kai L,Kaldenhoff R.Plant aquaporins and CO2[M]//In:Chaumont F,Tyerman S eds.Plant aquaporins.Signaling and Communication in Plant.Switzerland:Springer International Publishing AG,Cham,2017:255-65
[6]Raven JA,Beardall J,Giordano M.Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms.Photosynth Res,2014,121:111-24
[7]Cornwall CE,Revill AT,Hurd CL.High prevalence of diffusive uptake of CO2 by macroalgae in a temperate subtidal ecosystem.Photosynth Res,2015,124:181-90
[8]Longphuirt SN,Eschmann C,Russell C,et al.Seasonal and species-specific response of five brown macroalgae to high atmospheric CO2.Mar Ecol Prog Ser,2013,493:91-102
[9]Jolliffe EA,Tregunna EB.Studies on HCO-3 ion uptake during photosynthesis in benthic marine algae.Phycologia,1970,9:293-303
[10]Larsson C,Axelsson L.Bicarbonate uptake and utilization in marine macroalgae.Eur J Phycol,1999,34:79-86
[11]岳国峰,戢勇骋,王建飞,等.海带雌配子体对无机碳的利用.海洋科学,2000,24:33-6
[12]ZouDH,GaoKS.Comparative mechanisms of photosynthetic carbon acquisition in Hizikia fusiforme under submersed and emersed conditions.Acta Bot Sin,2004,46:1178-85
[13]Quadir A,Harrison PJ,DeWreede RE.The effects of emergence and submergence on the photosynthesis and respiration of marine macrophytes.Phycologia,1979,18:83-8
[14]Bidwell RGS,McLachlan J.Carbon nutrition of seaweeds:photosynthesis,photorespiration and respiration.J Exp Mar Biol Ecol,1985,86:15-46
[15]Raven JA,Ball LA,Beardall J,et al.Algae lacking carbon-concentrating mechanisms.Can J Bot,2005,83:879-90
[16]Maberly SC,Raven JA,Johnston AM.Discrimination between 12C and 13C by marine plants.Oecologia,1992,91:481-92
[17]Maberly SC.Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae.J Phycol,1990,26:439-49
[18]岳国峰,王金霞,朱明远,等.藻类无机碳的研究进展(I)--研究起源及研究方法.海洋科学,2003,27:15-8
[19]Fernández PA,Roleda MY,Rautenberger R,et al.Carbonic anhydraseactivity in sea weeds:over view and recommendations recommendations for measuring activity with an electrometric method,using Macrocystis pyrifera as a model species.Mar Biol,2018,165:88
[20]Sand-Jensen K,Gordon DM.Differential ability of marine and freshwater macrophytes to utilize HCO-3 and CO2.Mar Biol,1984,80:247-53
[21]Cook CM,Lanaras T,Colman B.Evidence for bicarbonate transport in species of red and brown macrophytic marine algae.J Exp Bot,1986,37:977-84
[22]Surif MB,Raven JA.Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and Laminariales(Phaeophyta):ecological and taxonomic implications.Oecologia,1989,78:97-105
[23]Mercado JM,Gordillo FJL,Figueroa FL,et al.External carbonic anhydrase and affinity for inorganic carbon in intertidal macroalgae.J Exp Mar Biol Ecol,1998,221:209-20
[24]Schmid R.Photosynthesis of Ectocarpus siliculosus in red light and after pulses of blue light at high pH-evidence for bicarbonate uptake.Plant Cell Environ,1998,21:523-9
[25]Haglund K,Ramazanov Z,Mtolera M,et al.Role of external carbonic anhydrase in light-dependent alkalization by Fucus serratus L.and Laminaria saccharina(L.)Lamour.(Phaeophyta).Planta,1992,188:1-6
[26]Zou D,Gao K,Xia J.Photosynthetic utilization of inorganic carbon in the economic brown alga,Hizikia fusiforme(Sargassaceae)from the south China sea.J Phycol,2003,39:1095-100
[27]Zou D,Gao K,Chen W.Photosynthetic carbon acquisition in Sargassum henslowianum(Fucales,Phaeophyta),with special reference to the comparison between the vegetative and reproductive tissues.Photosynth Res,2011,107:159-68
[28]Klenell M,Snoeijs P,Pedersén M.The involvement of aplasmamem braneH+-ATPasein the blue-light enhancement of photosynthesis in Laminaria digitata(Phaeophyta).J Phycol,2002,38:1143-9
[29]Klenell M,Snoeijs P,Pedersén M.Active carbon uptake in Laminaria digitata and L.saccharina(Phaeophyta)is driven by a proton pump in the plasma membrane.Hydrobiologia,2004,514:41-53
[30]García-Sánchez MJ,Delgado-Huertas A,Fernández JA,et al.Photosynthetic use of inorganic carbon in deep-water kelps from the Strait of Gibraltar.Photosynth Res,2016,127:295-305
[31]Fernández PA,Hurd CL,Roleda MY.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,2014,50:998-1008
[32]Flores-Moya A,Fernández JA.The role of external carbonic anhydrase in the photosynthetic use of inorganic carbon in the deep-water alga Phyllariopsis purpurascens(Laminariales,Phaeophyta).Planta,1998,207:115-9
[33]岳国峰,王金霞,王建飞,等.海带幼孢子体的光合碳利用.海洋与湖沼,2001,32:647-52
[34]Axelsson L,Mercado JM,Figueroa FL.Utilization of HCO-3 at high pH by the brown macroalga Laminaria saccharina.Eur J Phycol,2000,35:53-9
[35]Zhang X,Hu H,Tan T.Photosynthetic inorganic carbon utilization of gametophytes and sporophytes of Undaria pinnatifida(Phaeophyceae).Phycologia,2006,45:642-7
[36]Zou D,Gao K.Acquisition of inorganic carbon by Endarachne binghamiae(Scytosiphonales,Phaeophyceae).Eur J Phycol,2010,45:117-26
[37]Drechsler Z,Sharkia R,Cabantchik ZI,et al.Bicarbonate uptake in the marine macroaiga Ulva sp.is inhibited by classical probes of anion exchange by red blood cells.Planta,1993,191:34-40
[38]Ikemori M,Nishida K.Carbonic anhydrase in the marine alga Ulva pertusa.Physiol Plant,1968,21:292-7
[39]Karlsson J,Ramazanov Z,Hiltonen T,et al.Effect of vanadate on photosynthesis and the ATP/ADP ratio in low-CO2-adapted Chlamydomorms reinhardtii cells.Planta,1994,192:46-51
[40]Johnston AM.The acquisition of inorganic carbon by marine macroalgae.Can J Bot,1991,69:1123-32
[41]邹定辉,高坤山.大型海藻类光合无机碳利用研究进展.海洋通报,2001,20:83-90
[42]Badger MR.The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms.Photosynth Res,2003,77:83-94
[43]Raven JA,Hurd CL.Ecophysiology of photosynthesis in macroalgae.Photosynth Res,2012,113:105-25
[44]Cannon GC,Heinhorst S,Kerfeld CA.Carboxysomal carbonic anhydrases:Structure and role in microbial CO2fixation.Biochim Biophys Acta,2010,1804:382-92
[45]Moroney JV,Ma Y,Frey WD,et al.The carbonic anhydrase isoforms of Chlamydomonas reinhardtii:intracellular location,expression,and physiological roles.Photosynth Res,2011,109:133-49
[46]Mercado JM,Andría JR,Pérez-Llorens JL,et al.Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina.Photosynth Res,2006,88:259-68
[47]Kremer BP.Metabolic implications of non-photosynthetic carbon fixation in brown macroalgae.Phycologia,1981,20:242-50
[48]侯和胜,姚南瑜.海带磷酸烯醇式丙酮酸羧激酶的提取和特性.植物生理学通讯,1991,27:100-3
[49]Cabello-Pasini A,Alberte RS.Expression of carboxylating enzymes in Laminaria setchellii(Phaeophyceae).Phycologia,2001,40:351-8
[50]Kawamitsu Y,Boyer JS.Photosynthesis and carbon storage between tides in a brown alga,Fucus vesiculosus.Mar Biol,1999,133:361-9
[51]Schmid R,Dring MJ.Influence of carbon supply on the circadian rhythmicity of photosynthesis and its stimulation by blue light in Ectocarpus siliculosus:clues to the mechanism of inorganic carbon acquisition in lower brown algae.Plant Cell Environ,1996,19:373-82
[52]Bi YH,Li JL,Zhou ZG.Full-length mRNA sequencing in Saccharina japonica and identification of carbonic anhydrase genes.Aquacult Fish,2019,4:53-60
[53]Cock JM,Sterck L,RouzéP,et al.The Ectocarpus genome and the independent evolution of multicellularity in brown algae.Nature,2010,465:617-21
[54]Hopkinson BM,Dupont CL,Matsuda Y.The physiology and genetics of CO2 concentrating mechanisms in model diatoms.Curr Opin Plant Biol,2016,31:51-7
[55]Ye RX,Yu Z,Shi WW,et al.Characterization ofα-type carbonic anhydrase(CA)gene and subcellular localization ofα-CA in the gametophytes of Saccharina japonica.JAppl Phycol,2014,26:881-90
[56]Trimborn S,Wolf-Gladrow D,Richter K-U,et al.The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms.J Exp Mar Biol Ecol,2009,376:26-36
[57]Meldrum NU,Roughton FJW.Carbonic anhydrase.Its preparation and properties.J Physiol,1933,80:113-42
[58]Tsuji Y,Nakajima K,Matsuda Y.Molecular aspects of the biophysical CO2-concentrating mechanism and its regulation in marine diatoms.J Exp Bot,2017,68:3763-72
[59]Brinkman R.The occurrence of carbonic anhydrase in lower marine animals.J Physiol,1934,80:171-3
[60]Bowes GW.Carbonic anhydrase in marine algae.Plant Physiol,1969,44:726-32
[61]Graham D,Smillie RM.Carbonate dehydratase in marine organisms of the Great Barrier Reef.Aust J Plant Physiol,1976,3:113-9
[62]Giordano M,Maberly SC.Distribution of carbonic anhydrase in British marine macroalgae.Oecologia,1989,81:534-9
[63]Gordillo FJL,Aguilera J,Jiménez C.The response of nutrient assimilation and biochemical composition of Arctic seaweeds to a nutrient input in summer.J Exp Bot,2006,57:2661-71
[64]Zou D,Gao K.Photosynthetic acclimation to different light levels in the brown marine macroalga,Hizikia fusiformis(Sargassaceae,Phaeophyta).J Appl Phycol,2010,22:395-404
[65]Mercado JM,Figueroa FL,Niell FX,et al.A new method for estimating external carbonic anhydrase activity in macroalgae.J Phycol,1997,33:999-1006
[66]Huovinen P,Gómez I,Orostegui M.Patterns and UVsensitivity of carbon anhydrase and nitrate reductase activities in south Pacific macroalgae.Mar Biol,2007,151:1813-21
[67]Wilbur KM,Anderson NG.Electrometric and colorimetric determination of carbonic anhydrase.J Biol Chem,1948,176:147-54
[68]Okazaki M.Dissociable zinc as a cofactor of carbonic anhydrase from the marine red alga Serraticardia maxima.Bot Mag,1973,86:235-9
[69]Fernández PA,Roleda MY,Hurd CL.Effects of ocean acidification on the photosynthetic performance,carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera.Photosynth Res,2015,124:293-304
[70]Zou D.Effects of elevated atmospheric CO2 on growth,photosynthesis and nitrogen metabolism in the economic brown seaweed,Hizikia fusiforme(Sargassaceae,Phaeophyta).Aquaculture,2005,250:726-35
[71]Vi?egla B,Segovia M,Figueroa FL.Effect of artificial UVradiation on carbon and nitrogen metabolism in the macroalgae Fucus spiralis L.and Ulva olivascens Dangeard.Hydrobiologia,2006,560:31-42
[72]Gordillo FJL,Aguilera J,Wiencke C,et al.Ocean acidification modulates the response of two Arctic kelps to ultraviolet radiation.J Plant Physiol,2015,173:41-50
[73]Haglund K,Bj?rk M,Ramazanov Z,et al.Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata.Planta,1992,187:275-81
[74]Mercado JM,Vi?egla B,Figueroa FL,et al.Isoenzymic forms of carbonic anhydrase in the red macroalga Porphyra leucosticta.Physiol Plant,1999,106:69-74
[75]Andría JR,Vergara JJ,Pérez-Lloréns JL.Fractionation of carbonic anhydrase activity in Gracilaria sp.(Rhodophyta)and Enteromorpha intestinalis(Chlorophyta):changes in the extracellular activity in response to inorganic carbon levels.Aust J Plant Physiol,2000,27:1161-7
[76]Gómez-Pinchetti JL,Ramazanov Z,Garcia-Reina G.Effect of inhibitors of carbonic anhydrase activity on photosynthesis in the red alga Soliera filiformis(Gigartinales:Rodophyta).Mar Biol,1992,114:335-9
[77]Moulin P,Crépineau F,Kloareg B,et al.Isolation and characterization of six cDNAs involved in carbon metabolism in Laminaria digitata(Phaeophyceae).J Phycol,1999,35:1237-45
[78]余贞,毕燕会,周志刚.海带配子体碳酸酐酶(CA)基因的克隆及其特征分析.水产学报,2011,35:1343-53
[79]Ye N,Zhang X,Miao M,et al.Saccharina genomes provide novel insight into kelp biology.Nat Commun,2015,6:6986
[80]Deng YY,Yao JT,Wang XL.Transcriptome sequencing and comparative analysis of Saccharina japonica(Laminariales,Phaeophyceae)under blue light induction.PLoS One,2012,7:e39704
[81]Wang WJ,Wang FJ,Sun XT.Comparison of transcriptome under red and blue light culture of Saccharina japonica(Phaeophyceae).Planta,2013,237:1123-33
[82]Heinrich S,Valentin K,Frickenhaus S.Transcriptomic analysis of acclimation to temperature and light stress in Saccharina latissima(Phaeophyceae).PLoS One,2012,7:e44342
[83]Bi YH,Zhou ZG.Absorption and transport of inorganic carbon in kelps with emphasis on Saccharina japonica[M]//In:Najafpour MM ed.Applied Photosynthesis-New Progress.Croatia:InTech,51000 Rijeka,2016,111-31
[84]Floryszak-Wieczorek J,Arasimowicz-Jelonek M.The multifunctional face of plant carbonic anhydrase.Plant Physiol Biochem,2017,112:362-8
[85]Gao K,McKinley KR.Use of macroalgae for marine biomass production-a review.J Appl Phycol,1994,6:45-60
[86]Ross AB,Jones JM,Kubacki ML,et al.Classification of macroalgae as fuel and its thermochemical behaviour.Bioresour Technol,2008,99:6494-504
[2]Taiz L,Zeiger E.Plant Physiology[M].5th Ed.Sunderland:Sinauer Associates Inc.,2010:67-83
[3]Raven JA.Inorganic carbon acquisition by marine autotrophs.Adv Bot Res,1997,27:85-209
[4]Bartsch I,Wiencke C,Bischof K,et al.The genus Laminaria sensu lato:recent insights and developments.Eur J Phycol,2008,43:1-86
[5]Uehlein N,Kai L,Kaldenhoff R.Plant aquaporins and CO2[M]//In:Chaumont F,Tyerman S eds.Plant aquaporins.Signaling and Communication in Plant.Switzerland:Springer International Publishing AG,Cham,2017:255-65
[6]Raven JA,Beardall J,Giordano M.Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms.Photosynth Res,2014,121:111-24
[7]Cornwall CE,Revill AT,Hurd CL.High prevalence of diffusive uptake of CO2 by macroalgae in a temperate subtidal ecosystem.Photosynth Res,2015,124:181-90
[8]Longphuirt SN,Eschmann C,Russell C,et al.Seasonal and species-specific response of five brown macroalgae to high atmospheric CO2.Mar Ecol Prog Ser,2013,493:91-102
[9]Jolliffe EA,Tregunna EB.Studies on HCO-3 ion uptake during photosynthesis in benthic marine algae.Phycologia,1970,9:293-303
[10]Larsson C,Axelsson L.Bicarbonate uptake and utilization in marine macroalgae.Eur J Phycol,1999,34:79-86
[11]岳国峰,戢勇骋,王建飞,等.海带雌配子体对无机碳的利用.海洋科学,2000,24:33-6
[12]ZouDH,GaoKS.Comparative mechanisms of photosynthetic carbon acquisition in Hizikia fusiforme under submersed and emersed conditions.Acta Bot Sin,2004,46:1178-85
[13]Quadir A,Harrison PJ,DeWreede RE.The effects of emergence and submergence on the photosynthesis and respiration of marine macrophytes.Phycologia,1979,18:83-8
[14]Bidwell RGS,McLachlan J.Carbon nutrition of seaweeds:photosynthesis,photorespiration and respiration.J Exp Mar Biol Ecol,1985,86:15-46
[15]Raven JA,Ball LA,Beardall J,et al.Algae lacking carbon-concentrating mechanisms.Can J Bot,2005,83:879-90
[16]Maberly SC,Raven JA,Johnston AM.Discrimination between 12C and 13C by marine plants.Oecologia,1992,91:481-92
[17]Maberly SC.Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae.J Phycol,1990,26:439-49
[18]岳国峰,王金霞,朱明远,等.藻类无机碳的研究进展(I)--研究起源及研究方法.海洋科学,2003,27:15-8
[19]Fernández PA,Roleda MY,Rautenberger R,et al.Carbonic anhydraseactivity in sea weeds:over view and recommendations recommendations for measuring activity with an electrometric method,using Macrocystis pyrifera as a model species.Mar Biol,2018,165:88
[20]Sand-Jensen K,Gordon DM.Differential ability of marine and freshwater macrophytes to utilize HCO-3 and CO2.Mar Biol,1984,80:247-53
[21]Cook CM,Lanaras T,Colman B.Evidence for bicarbonate transport in species of red and brown macrophytic marine algae.J Exp Bot,1986,37:977-84
[22]Surif MB,Raven JA.Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and Laminariales(Phaeophyta):ecological and taxonomic implications.Oecologia,1989,78:97-105
[23]Mercado JM,Gordillo FJL,Figueroa FL,et al.External carbonic anhydrase and affinity for inorganic carbon in intertidal macroalgae.J Exp Mar Biol Ecol,1998,221:209-20
[24]Schmid R.Photosynthesis of Ectocarpus siliculosus in red light and after pulses of blue light at high pH-evidence for bicarbonate uptake.Plant Cell Environ,1998,21:523-9
[25]Haglund K,Ramazanov Z,Mtolera M,et al.Role of external carbonic anhydrase in light-dependent alkalization by Fucus serratus L.and Laminaria saccharina(L.)Lamour.(Phaeophyta).Planta,1992,188:1-6
[26]Zou D,Gao K,Xia J.Photosynthetic utilization of inorganic carbon in the economic brown alga,Hizikia fusiforme(Sargassaceae)from the south China sea.J Phycol,2003,39:1095-100
[27]Zou D,Gao K,Chen W.Photosynthetic carbon acquisition in Sargassum henslowianum(Fucales,Phaeophyta),with special reference to the comparison between the vegetative and reproductive tissues.Photosynth Res,2011,107:159-68
[28]Klenell M,Snoeijs P,Pedersén M.The involvement of aplasmamem braneH+-ATPasein the blue-light enhancement of photosynthesis in Laminaria digitata(Phaeophyta).J Phycol,2002,38:1143-9
[29]Klenell M,Snoeijs P,Pedersén M.Active carbon uptake in Laminaria digitata and L.saccharina(Phaeophyta)is driven by a proton pump in the plasma membrane.Hydrobiologia,2004,514:41-53
[30]García-Sánchez MJ,Delgado-Huertas A,Fernández JA,et al.Photosynthetic use of inorganic carbon in deep-water kelps from the Strait of Gibraltar.Photosynth Res,2016,127:295-305
[31]Fernández PA,Hurd CL,Roleda MY.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,2014,50:998-1008
[32]Flores-Moya A,Fernández JA.The role of external carbonic anhydrase in the photosynthetic use of inorganic carbon in the deep-water alga Phyllariopsis purpurascens(Laminariales,Phaeophyta).Planta,1998,207:115-9
[33]岳国峰,王金霞,王建飞,等.海带幼孢子体的光合碳利用.海洋与湖沼,2001,32:647-52
[34]Axelsson L,Mercado JM,Figueroa FL.Utilization of HCO-3 at high pH by the brown macroalga Laminaria saccharina.Eur J Phycol,2000,35:53-9
[35]Zhang X,Hu H,Tan T.Photosynthetic inorganic carbon utilization of gametophytes and sporophytes of Undaria pinnatifida(Phaeophyceae).Phycologia,2006,45:642-7
[36]Zou D,Gao K.Acquisition of inorganic carbon by Endarachne binghamiae(Scytosiphonales,Phaeophyceae).Eur J Phycol,2010,45:117-26
[37]Drechsler Z,Sharkia R,Cabantchik ZI,et al.Bicarbonate uptake in the marine macroaiga Ulva sp.is inhibited by classical probes of anion exchange by red blood cells.Planta,1993,191:34-40
[38]Ikemori M,Nishida K.Carbonic anhydrase in the marine alga Ulva pertusa.Physiol Plant,1968,21:292-7
[39]Karlsson J,Ramazanov Z,Hiltonen T,et al.Effect of vanadate on photosynthesis and the ATP/ADP ratio in low-CO2-adapted Chlamydomorms reinhardtii cells.Planta,1994,192:46-51
[40]Johnston AM.The acquisition of inorganic carbon by marine macroalgae.Can J Bot,1991,69:1123-32
[41]邹定辉,高坤山.大型海藻类光合无机碳利用研究进展.海洋通报,2001,20:83-90
[42]Badger MR.The roles of carbonic anhydrases in photosynthetic CO2 concentrating mechanisms.Photosynth Res,2003,77:83-94
[43]Raven JA,Hurd CL.Ecophysiology of photosynthesis in macroalgae.Photosynth Res,2012,113:105-25
[44]Cannon GC,Heinhorst S,Kerfeld CA.Carboxysomal carbonic anhydrases:Structure and role in microbial CO2fixation.Biochim Biophys Acta,2010,1804:382-92
[45]Moroney JV,Ma Y,Frey WD,et al.The carbonic anhydrase isoforms of Chlamydomonas reinhardtii:intracellular location,expression,and physiological roles.Photosynth Res,2011,109:133-49
[46]Mercado JM,Andría JR,Pérez-Llorens JL,et al.Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina.Photosynth Res,2006,88:259-68
[47]Kremer BP.Metabolic implications of non-photosynthetic carbon fixation in brown macroalgae.Phycologia,1981,20:242-50
[48]侯和胜,姚南瑜.海带磷酸烯醇式丙酮酸羧激酶的提取和特性.植物生理学通讯,1991,27:100-3
[49]Cabello-Pasini A,Alberte RS.Expression of carboxylating enzymes in Laminaria setchellii(Phaeophyceae).Phycologia,2001,40:351-8
[50]Kawamitsu Y,Boyer JS.Photosynthesis and carbon storage between tides in a brown alga,Fucus vesiculosus.Mar Biol,1999,133:361-9
[51]Schmid R,Dring MJ.Influence of carbon supply on the circadian rhythmicity of photosynthesis and its stimulation by blue light in Ectocarpus siliculosus:clues to the mechanism of inorganic carbon acquisition in lower brown algae.Plant Cell Environ,1996,19:373-82
[52]Bi YH,Li JL,Zhou ZG.Full-length mRNA sequencing in Saccharina japonica and identification of carbonic anhydrase genes.Aquacult Fish,2019,4:53-60
[53]Cock JM,Sterck L,RouzéP,et al.The Ectocarpus genome and the independent evolution of multicellularity in brown algae.Nature,2010,465:617-21
[54]Hopkinson BM,Dupont CL,Matsuda Y.The physiology and genetics of CO2 concentrating mechanisms in model diatoms.Curr Opin Plant Biol,2016,31:51-7
[55]Ye RX,Yu Z,Shi WW,et al.Characterization ofα-type carbonic anhydrase(CA)gene and subcellular localization ofα-CA in the gametophytes of Saccharina japonica.JAppl Phycol,2014,26:881-90
[56]Trimborn S,Wolf-Gladrow D,Richter K-U,et al.The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms.J Exp Mar Biol Ecol,2009,376:26-36
[57]Meldrum NU,Roughton FJW.Carbonic anhydrase.Its preparation and properties.J Physiol,1933,80:113-42
[58]Tsuji Y,Nakajima K,Matsuda Y.Molecular aspects of the biophysical CO2-concentrating mechanism and its regulation in marine diatoms.J Exp Bot,2017,68:3763-72
[59]Brinkman R.The occurrence of carbonic anhydrase in lower marine animals.J Physiol,1934,80:171-3
[60]Bowes GW.Carbonic anhydrase in marine algae.Plant Physiol,1969,44:726-32
[61]Graham D,Smillie RM.Carbonate dehydratase in marine organisms of the Great Barrier Reef.Aust J Plant Physiol,1976,3:113-9
[62]Giordano M,Maberly SC.Distribution of carbonic anhydrase in British marine macroalgae.Oecologia,1989,81:534-9
[63]Gordillo FJL,Aguilera J,Jiménez C.The response of nutrient assimilation and biochemical composition of Arctic seaweeds to a nutrient input in summer.J Exp Bot,2006,57:2661-71
[64]Zou D,Gao K.Photosynthetic acclimation to different light levels in the brown marine macroalga,Hizikia fusiformis(Sargassaceae,Phaeophyta).J Appl Phycol,2010,22:395-404
[65]Mercado JM,Figueroa FL,Niell FX,et al.A new method for estimating external carbonic anhydrase activity in macroalgae.J Phycol,1997,33:999-1006
[66]Huovinen P,Gómez I,Orostegui M.Patterns and UVsensitivity of carbon anhydrase and nitrate reductase activities in south Pacific macroalgae.Mar Biol,2007,151:1813-21
[67]Wilbur KM,Anderson NG.Electrometric and colorimetric determination of carbonic anhydrase.J Biol Chem,1948,176:147-54
[68]Okazaki M.Dissociable zinc as a cofactor of carbonic anhydrase from the marine red alga Serraticardia maxima.Bot Mag,1973,86:235-9
[69]Fernández PA,Roleda MY,Hurd CL.Effects of ocean acidification on the photosynthetic performance,carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera.Photosynth Res,2015,124:293-304
[70]Zou D.Effects of elevated atmospheric CO2 on growth,photosynthesis and nitrogen metabolism in the economic brown seaweed,Hizikia fusiforme(Sargassaceae,Phaeophyta).Aquaculture,2005,250:726-35
[71]Vi?egla B,Segovia M,Figueroa FL.Effect of artificial UVradiation on carbon and nitrogen metabolism in the macroalgae Fucus spiralis L.and Ulva olivascens Dangeard.Hydrobiologia,2006,560:31-42
[72]Gordillo FJL,Aguilera J,Wiencke C,et al.Ocean acidification modulates the response of two Arctic kelps to ultraviolet radiation.J Plant Physiol,2015,173:41-50
[73]Haglund K,Bj?rk M,Ramazanov Z,et al.Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata.Planta,1992,187:275-81
[74]Mercado JM,Vi?egla B,Figueroa FL,et al.Isoenzymic forms of carbonic anhydrase in the red macroalga Porphyra leucosticta.Physiol Plant,1999,106:69-74
[75]Andría JR,Vergara JJ,Pérez-Lloréns JL.Fractionation of carbonic anhydrase activity in Gracilaria sp.(Rhodophyta)and Enteromorpha intestinalis(Chlorophyta):changes in the extracellular activity in response to inorganic carbon levels.Aust J Plant Physiol,2000,27:1161-7
[76]Gómez-Pinchetti JL,Ramazanov Z,Garcia-Reina G.Effect of inhibitors of carbonic anhydrase activity on photosynthesis in the red alga Soliera filiformis(Gigartinales:Rodophyta).Mar Biol,1992,114:335-9
[77]Moulin P,Crépineau F,Kloareg B,et al.Isolation and characterization of six cDNAs involved in carbon metabolism in Laminaria digitata(Phaeophyceae).J Phycol,1999,35:1237-45
[78]余贞,毕燕会,周志刚.海带配子体碳酸酐酶(CA)基因的克隆及其特征分析.水产学报,2011,35:1343-53
[79]Ye N,Zhang X,Miao M,et al.Saccharina genomes provide novel insight into kelp biology.Nat Commun,2015,6:6986
[80]Deng YY,Yao JT,Wang XL.Transcriptome sequencing and comparative analysis of Saccharina japonica(Laminariales,Phaeophyceae)under blue light induction.PLoS One,2012,7:e39704
[81]Wang WJ,Wang FJ,Sun XT.Comparison of transcriptome under red and blue light culture of Saccharina japonica(Phaeophyceae).Planta,2013,237:1123-33
[82]Heinrich S,Valentin K,Frickenhaus S.Transcriptomic analysis of acclimation to temperature and light stress in Saccharina latissima(Phaeophyceae).PLoS One,2012,7:e44342
[83]Bi YH,Zhou ZG.Absorption and transport of inorganic carbon in kelps with emphasis on Saccharina japonica[M]//In:Najafpour MM ed.Applied Photosynthesis-New Progress.Croatia:InTech,51000 Rijeka,2016,111-31
[84]Floryszak-Wieczorek J,Arasimowicz-Jelonek M.The multifunctional face of plant carbonic anhydrase.Plant Physiol Biochem,2017,112:362-8
[85]Gao K,McKinley KR.Use of macroalgae for marine biomass production-a review.J Appl Phycol,1994,6:45-60
[86]Ross AB,Jones JM,Kubacki ML,et al.Classification of macroalgae as fuel and its thermochemical behaviour.Bioresour Technol,2008,99:6494-504