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海洋酸化与磷限制对颗石藻(Emiliania huxleyi)生理特征的耦合效应

马帅 张泳 杨祥 王茵蕊 谢蓉蓉 李家兵 张虹 韩永和 张勇

马帅,张泳,杨祥,等. 海洋酸化与磷限制对颗石藻(Emiliania huxleyi)生理特征的耦合效应[J]. 海洋学报,2023,45(8):120–129 doi: 10.12284/hyxb2023108
引用本文: 马帅,张泳,杨祥,等. 海洋酸化与磷限制对颗石藻(Emiliania huxleyi)生理特征的耦合效应[J]. 海洋学报,2023,45(8):120–129 doi: 10.12284/hyxb2023108
Ma Shuai,Zhang Yong,Yang Xiang, et al. Combined effects of ocean acidification and phosphorus limitation on physiological characteristics of the coccolithophores Emiliania huxleyi[J]. Haiyang Xuebao,2023, 45(8):120–129 doi: 10.12284/hyxb2023108
Citation: Ma Shuai,Zhang Yong,Yang Xiang, et al. Combined effects of ocean acidification and phosphorus limitation on physiological characteristics of the coccolithophores Emiliania huxleyi[J]. Haiyang Xuebao,2023, 45(8):120–129 doi: 10.12284/hyxb2023108

海洋酸化与磷限制对颗石藻(Emiliania huxleyi)生理特征的耦合效应

doi: 10.12284/hyxb2023108
基金项目: 福建省自然科学基金面上项目(2023J01290);国家自然科学基金青年项目(41806129)。
详细信息
    作者简介:

    马帅(1997-),男,河南省长葛市人,主要从事海洋藻类生理学研究。E-mail: ms1471692021@163.com

    通讯作者:

    张勇,男,副研究员,主要研究海洋微藻响应气候变化的生理生态特征及其机制。E-mail: yongzhang@fjnu.edu.cn

  • 中图分类号: P714+.5;Q949.2

Combined effects of ocean acidification and phosphorus limitation on physiological characteristics of the coccolithophores Emiliania huxleyi

  • 摘要: 颗石藻既通过光合作用合成颗粒有机碳(POC),又通过钙化作用产生颗粒无机碳(PIC),对海洋碳循环有重要贡献。虽然已有一些研究报道海洋酸化通常可增加颗石藻细胞POC含量,减少细胞PIC含量,但是这些实验结果大部分是在营养盐浓度充足条件下获得,且较少研究关注营养盐浓度限制和海洋酸化对颗石藻的耦合作用。本文研究了在无机磷浓度限制条件下,赫氏颗石藻(Emiliania huxleyi)的主要生理指标对海洋酸化的响应特征。结果显示,海洋酸化和无机磷浓度限制协同降低了颗石藻的生长速率、相对电子传递速率和光能利用效率。无机磷浓度限制主导增加颗石藻的光合固碳量,并抵消了海洋酸化对细胞PIC含量及PIC/POC比率的负面效应。研究结果表明,无机磷浓度限制改变了颗石藻的两种固碳作用对海洋酸化的响应趋势,暗示在无机磷浓度不同的海域,颗石藻对海洋碳循环的贡献不同。
  • 图  1  不同处理下,在培养开始和结束时,培养基中溶解无机磷(DIP)浓度(A−D)、CO2分压(E−H)、pH(I−L)和细胞浓度(单位:cell/mL)的自然对数(M−P)

    Fig.  1  Dissolved inorganic phosphorus (DIP) concentration (A−D), pCO2 level (E−H), pH (I−L) and logarithm of cell concentration (unit: cell/mL) (M−P) at the beginning and end of the cultures under different treatments

    图  2  不同处理下赫氏颗石藻(Emiliania huxleyi)株系RCC1266的生长速率(A)、叶绿素a含量(B)、类胡萝卜素含量(C)及类胡萝卜素与叶绿素a含量的比率(D)

    不同字母代表显著性差异

    Fig.  2  Growth rate (A), chlorophyll a content (B), carotenoid content (C) and the ratio of carotenoid content to chlorophyll a content (D) of the coccolithophore Emiliania huxleyi RCC1266 under different treatments

    Different letters represent significant difference

    图  3  不同处理下赫氏颗石藻(Emiliania huxleyi)株系RCC1266相对电子传递速率(rETR)对检测光强的响应曲线(A)、最大相对电子传递速率 (rETRmax)(B)、光能利用效率(α)(C)和半饱和光强 (Ik)(D)

    不同字母表示显著性差异

    Fig.  3  Relative electron transport rate (rETR) as a function of the assay light intensity (A), maximal relative electron transport rate (rETRmax) (B), light use efficiency (α) (C) and half-saturating light intensity (Ik) (D) of the coccolithophore Emiliania huxleyi RCC1266 under different treatments

    Different letters represent significant difference

    图  4  不同处理下赫氏颗石藻(Emiliania huxleyi)株系RCC1266细胞颗粒无机碳(PIC)含量(A)、颗粒有机碳(POC)含量(B)和颗粒无机碳与颗粒有机碳(PIC/POC)的比率(C)

    不同字母代表显著性差异

    Fig.  4  The cellular particulate inorganic carbon (PIC) content (A), particulate organic carbon (POC) content (B) and the ratio of PIC to POC (PIC/POC) (C) of the coccolithophore Emiliania huxleyi RCC1266 under different treatments

    Different letters represent significant difference

    表  1  二元方差分析获得无机磷浓度和CO2浓度及其相互作用对赫氏颗石藻(Emiliania huxleyi)株系RCC1266的生长速率、色素含量、荧光参数、细胞元素含量及其比率影响的统计结果

    Tab.  1  Results of two-way ANOVA of the effects of inorganic phosphorus concentration and CO2 concentration and their interactions on growth rate, pigment content, fluorescence parameters, cellular elements content and their ratios of the coccolithophore Emiliania huxleyi RCC1266

    无机磷浓度CO2浓度无机磷浓度和CO2浓度
    FpFpFp
    生长速率/d−1281.76< 0.001218.75< 0.001196.08< 0.001
    叶绿素a含量/( pg·cell−1)0.140.7209.600.01512.510.008
    类胡萝卜素含量/( pg·cell−1)12.700.0076.48 0.03417.940.003
    类胡萝卜素与叶绿素a含量的比率8.440.0202.700.1391.04 0.338
    最大相对电子传递速率29.99< 0.001239.26< 0.001157.10< 0.001
    光能利用效率136.70< 0.001229.46< 0.001343.01< 0.001
    半饱和光强/(μmol ·m−2 ·s−1)8.53 0.0190.010.9497.610.025
    颗粒无机碳含量/( pg·cell−1)42.52< 0.00118.26 0.0031.53 0.251
    颗粒有机碳含量/( pg·cell−1)68.46< 0.0012.75 0.1360.100.759
    颗粒无机碳与颗粒有机碳含量的比率12.110.00816.94 0.0031.68 0.231
    注:统计学的显著性差异通过p < 0.05来表达,此处的p值是数据整体分析的结果;颗粒无机碳含量和颗粒有机碳含量以碳计。
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  • [1] Friedlingstein P, Cox P, Betts R, et al. Climate-carbon cycle feedback analysis: results from the C4MIP model intercomparison[J]. Journal of Climate, 2006, 19(14): 3337−3353. doi: 10.1175/JCLI3800.1
    [2] Sabine C L, Feely R A, Gruber N, et al. The oceanic sink for anthropogenic CO2[J]. Science, 2004, 305(5682): 367−371. doi: 10.1126/science.1097403
    [3] Doney S C. Plankton in a warmer world[J]. Nature, 2006, 444(7120): 695−696. doi: 10.1038/444695a
    [4] Thingstad T F, Krom M D, Mantoura R F C, et al. Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean[J]. Science, 2005, 309(5737): 1068−1071. doi: 10.1126/science.1112632
    [5] Vidal M, Duarte C M, Agustí S, et al. Alkaline phosphatase activities in the central Atlantic Ocean indicate large areas with phosphorus deficiency[J]. Marine Ecology Progress Series, 2003, 262: 43−53. doi: 10.3354/meps262043
    [6] Krom M D, Kress N, Brenner S, et al. Phosphorus limitation of primary productivity in the eastern Mediterranean Sea[J]. Limnology and Oceanography, 1991, 36(3): 424−432. doi: 10.4319/lo.1991.36.3.0424
    [7] Shemi A, Schatz D, Fredricks H F, et al. Phosphorus starvation induces membrane remodeling and recycling in Emiliania huxleyi[J]. New Phytologist, 2016, 211(3): 886−898. doi: 10.1111/nph.13940
    [8] Meyer J, Riebesell U. Reviews and syntheses: responses of coccolithophores to ocean acidification: a meta-analysis[J]. Biogeosciences, 2015, 12(6): 1671−1682. doi: 10.5194/bg-12-1671-2015
    [9] 孙军. 今生颗石藻的有机碳泵和碳酸盐反向泵[J]. 地球科学进展, 2007, 22(12): 1231−1239. doi: 10.3321/j.issn:1001-8166.2007.12.003

    Sun Jun. Organic carbon pump and carbonate counter pump of living coccolithophorid[J]. Advances in Earth Science, 2007, 22(12): 1231−1239. doi: 10.3321/j.issn:1001-8166.2007.12.003
    [10] Balch W M, Holligan P M, Kilpatrick K A. Calcification, photosynthesis and growth of the bloom-forming coccolithophore, Emiliania huxleyi[J]. Continental Shelf Research, 1992, 12(12): 1353−1374. doi: 10.1016/0278-4343(92)90059-S
    [11] Xie Emei, Xu Kui, Li Zhengke, et al. Disentangling the effects of ocean carbonation and acidification on elemental contents and macromolecules of the coccolithophore Emiliania huxleyi[J]. Frontiers in Microbiology, 2021, 12: 737454. doi: 10.3389/fmicb.2021.737454
    [12] Riebesell U, Zondervan I, Rost B, et al. Reduced calcification of marine plankton in response to increased atmospheric CO2[J]. Nature, 2000, 407(6802): 364−367. doi: 10.1038/35030078
    [13] 廖晏, 冯媛媛, 刘瑶, 等. 氮限制和海洋酸化对颗石藻Emiliania huxleyi NIWA1108生理指标的交互影响[J]. 天津科技大学学报, 2019, 34(4): 56−62.

    Liao Yan, Feng Yuanyuan, Liu Yao, et al. Interactive effects of nitrogen limitation and ocean acidification on the physiology of coccolithophore Emiliania huxleyi NIWA1108[J]. Journal of Tianjin University of Science & Technology, 2019, 34(4): 56−62.
    [14] Duff S M G, Sarath G, Plaxton W C. The role of acid phosphatases in plant phosphorus metabolism[J]. Physiologia Plantarum, 1994, 90(4): 791−800. doi: 10.1111/j.1399-3054.1994.tb02539.x
    [15] Vagabov V M, Trilisenko L V, Kulaev I S. Dependence of inorganic polyphosphate chain length on the orthophosphate content in the culture medium of the yeast Saccharomyces cerevisiae[J]. Biochemistry, 2000, 65(3): 349−354.
    [16] Tyrrell T, Taylor A H. A modelling study of Emiliania huxleyi in the NE Atlantic[J]. Journal of Marine Systems, 1996, 9(1/2): 83−112.
    [17] Riegman R, Stolte W, Noordeloos A A M, et al. Nutrient uptake and alkaline phosphatase (ec 3: 1: 3: 1) activity of Emiliania huxleyi (PRYMNESIOPHYCEAE) during growth under n and p limitation in continuous cultures[J]. Journal of Phycology, 2000, 36(1): 87−96. doi: 10.1046/j.1529-8817.2000.99023.x
    [18] Oviedo A M, Langer G, Ziveri P. Effect of phosphorus limitation on coccolith morphology and element ratios in Mediterranean strains of the coccolithophore Emiliania huxleyi[J]. Journal of Experimental Marine Biology and Ecology, 2014, 459: 105−113. doi: 10.1016/j.jembe.2014.04.021
    [19] Berges J A, Franklin D J, Harrison P J. Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades[J]. Journal of Phycology, 2001, 37(6): 1138−1145. doi: 10.1046/j.1529-8817.2001.01052.x
    [20] Guillard R R L, Ryther J H. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran[J]. Canadian Journal of Microbiology, 1962, 8(2): 229−239. doi: 10.1139/m62-029
    [21] Hansen H P, Koroleff F. Determination of nutrients[M]//Grasshoff K, Kremling K, Ehrhardt M. Methods of Seawater Analysis. 3rd ed. New York: Wiley-VCH, 1999: 159−228.
    [22] Zhang Yong, Li Zhengke, Schulz K G, et al. Growth-dependent changes in elemental stoichiometry and macromolecular allocation in the coccolithophore Emiliania huxleyi under different environmental conditions[J]. Limnology and Oceanography, 2021, 66(8): 2999−3009. doi: 10.1002/lno.11854
    [23] Dickson A G, Afghan J D, Anderson G C. Reference materials for oceanic CO2 analysis: a method for the certification of total alkalinity[J]. Marine Chemistry, 2003, 80(2/3): 185−197.
    [24] Pierrot D E, Lewis E, Wallace D W R. MS Excel program developed for CO2 system calculations[R]. ORNL/CDIAC-105a. Oak Ridge, Tennessee: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U. S. Department of Energy, 2006.
    [25] Roy R N, Roy L N, Lawson M, et al. Thermodynamics of the dissociation of boric acid in seawater at S=35 from 0 to 55℃[J]. Marine Chemistry, 1993, 44(2/4): 243−248.
    [26] Jeffrey S W, Humphrey G F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton[J]. Biochemie und Physiologie der Pflanzen, 1975, 167(2): 191−194. doi: 10.1016/S0015-3796(17)30778-3
    [27] Davies B H. Carotenoids[M]//Goodwin T W. Chemistry and Biochemistry of Plant Pigments. London: Academic Press, 1976: 38−165.
    [28] Baker N R. Chlorophyll fluorescence: a probe of photosynthesis in vivo[J]. Annual Review of Plant Biology, 2008, 59: 89−113. doi: 10.1146/annurev.arplant.59.032607.092759
    [29] Ralph P J, Gademann R. Rapid light curves: a powerful tool to assess photosynthetic activity[J]. Aquatic Botany, 2005, 82(3): 222−237. doi: 10.1016/j.aquabot.2005.02.006
    [30] 高坤山. 藻类固碳——理论、进展与方法[M]. 北京: 科学出版社, 2014.

    Gao Kunshan. Algal Carbon Fixation: Basis, Advances and Methods[M]. Beijing: Science Press, 2014.
    [31] Smith H E K, Tyrrell T, Charalampopoulou A, et al. Predominance of heavily calcified coccolithophores at low CaCO3 saturation during winter in the Bay of Biscay[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(23): 8845−8849.
    [32] Wang Cong, Sun Xueqiong, Wang Jingtian, et al. Physiological and metabolic effects of glyphosate as the sole P source on a cosmopolitan phytoplankter and biogeochemical implications[J]. Science of the Total Environment, 2022, 832: 155094. doi: 10.1016/j.scitotenv.2022.155094
    [33] Fader C M, Colombo M I. Autophagy and multivesicular bodies: two closely related partners[J]. Cell Death & Differentiation, 2009, 16(1): 70−78.
    [34] Müller M, Schmidt O, Angelova M, et al. The coordinated action of the MVB pathway and autophagy ensures cell survival during starvation[J]. eLife, 2015, 4: e07736. doi: 10.7554/eLife.07736
    [35] Zhang Yong, Collins S, Gao Kunshan. Reduced growth with increased quotas of particulate organic and inorganic carbon in the coccolithophore Emiliania huxleyi under future ocean climate change conditions[J]. Biogeosciences, 2020, 17(24): 6357−6375. doi: 10.5194/bg-17-6357-2020
    [36] Zhang Yong, Zhang Yong, Ma Shuai, et al. Reallocation of elemental content and macromolecules in the coccolithophore Emiliania huxleyi to acclimate to climate change[J]. Biogeosciences, 2023, 20(7): 1299−1312. doi: 10.5194/bg-20-1299-2023
    [37] Rokitta S D, de Nooijer L J, Trimborn S, et al. Transcriptome analyses reveal differential gene expression patterns between the life-cycle stages of Emiliania huxleyi (Haptophyta) and reflect specialization to different ecological niches[J]. Journal of Phycology, 2011, 47(4): 829−838. doi: 10.1111/j.1529-8817.2011.01014.x
    [38] Rouco M, Branson O, Lebrato M, et al. The effect of nitrate and phosphate availability on Emiliania huxleyi (NZEH) physiology under different CO2 scenarios[J]. Frontiers in Microbiology, 2013, 4: 155.
    [39] Beardall J, Roberts S, Raven J A. Regulation of inorganic carbon acquisition by phosphorus limitation in the green alga Chlorella emersonii[J]. Canadian Journal of Botany, 2005, 83(7): 859−864. doi: 10.1139/b05-070
    [40] Rost B, Riebesell U. Coccolithophores and the biological pump: responses to environmental changes[M]//Thierstein H R, Young J R. Coccolithophores: From Molecular Processes to Global Impact. Berlin, Heidelberg: Springer, 2004: 99−125.
    [41] Jin Peng, Ding Jiancheng, Xing Tao, et al. High levels of solar radiation offset impacts of ocean acidification on calcifying and non-calcifying strains of Emiliania huxleyi[J]. Marine Ecology Progress Series, 2017, 568: 47−58. doi: 10.3354/meps12042
    [42] Li Zhengke, Dai Guozheng, Zhang Yong, et al. Photosynthetic adaptation to light availability shapes the ecological success of bloom-forming cyanobacterium Pseudanabaena to iron limitation[J]. Journal of Phycology, 2020, 56(6): 1457−1467. doi: 10.1111/jpy.13040
    [43] Li Hangxiao, Xu Tianpeng, Ma Jing, et al. Physiological responses of Skeletonema costatum to the interactions of seawater acidification and the combination of photoperiod and temperature[J]. Biogeosciences, 2021, 18(4): 1439−1449. doi: 10.5194/bg-18-1439-2021
    [44] Wang Cong, Wang Jingtian, Li Ling, et al. P-limitation promotes carbon accumulation and sinking of Emiliania huxleyi through transcriptomic reprogramming[J]. Frontiers in Marine Science, 2022, 9: 860222. doi: 10.3389/fmars.2022.860222
    [45] Wördenweber R, Rokitta S D, Heidenreich E, et al. Phosphorus and nitrogen starvation reveal life-cycle specific responses in the metabolome of Emiliania huxleyi (Haptophyta)[J]. Limnology and Oceanography, 2018, 63(1): 203−226. doi: 10.1002/lno.10624
    [46] Müller M N, Antia A N, LaRoche J. Influence of cell cycle phase on calcification in the coccolithophore Emiliania huxleyi[J]. Limnology and Oceanography, 2008, 53(2): 506−512. doi: 10.4319/lo.2008.53.2.0506
    [47] Zhang Yong, Fu Feixue, Hutchins D A, et al. Combined effects of CO2 level, light intensity, and nutrient availability on the coccolithophore Emiliania huxleyi[J]. Hydrobiologia, 2019, 842(1): 127−141. doi: 10.1007/s10750-019-04031-0
    [48] Langer G, Oetjen K, Brenneis T. Calcification of Calcidiscus leptoporus under nitrogen and phosphorus limitation[J]. Journal of Experimental Marine Biology and Ecology, 2012, 413: 131−137. doi: 10.1016/j.jembe.2011.11.028
    [49] Gerecht A C, Šupraha L, Edvardsen B, et al. High temperature decreases the PIC/POC ratio and increases phosphorus requirements in Coccolithus pelagicus (Haptophyta)[J]. Biogeosciences, 2014, 11(13): 3531−3545. doi: 10.5194/bg-11-3531-2014
    [50] Rokitta S D, John U, Rost B. Ocean acidification affects redox-balance and ion-homeostasis in the life-cycle stages of Emiliania huxleyi[J]. PLoS One, 2012, 7(12): e52212. doi: 10.1371/journal.pone.0052212
    [51] Langer G, Nehrke G, Probert I, et al. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry[J]. Biogeosciences, 2009, 6(11): 2637−2646. doi: 10.5194/bg-6-2637-2009
    [52] Fiorini S, Middelburg J J, Gattuso J P. Testing the effects of elevated pCO2 on coccolithophores (Prymnesiophyceae): comparison between haploid and diploid life stages[J]. Journal of Phycology, 2011, 47(6): 1281−1291. doi: 10.1111/j.1529-8817.2011.01080.x
    [53] Matthiessen B, Eggers S L, Krug S A. High nitrate to phosphorus regime attenuates negative effects of rising pCO2 on total population carbon accumulation[J]. Biogeosciences, 2012, 9(3): 1195−1203. doi: 10.5194/bg-9-1195-2012
    [54] Hoffmann R, Kirchlechner C, Langer G, et al. Insight into Emiliania huxleyi coccospheres by focused ion beam sectioning[J]. Biogeosciences, 2015, 12(3): 825−834. doi: 10.5194/bg-12-825-2015
    [55] Riebesell U, Bach L T, Bellerby R G J, et al. Competitive fitness of a predominant pelagic calcifier impaired by ocean acidification[J]. Nature Geoscience, 2017, 10(1): 19−23. doi: 10.1038/ngeo2854
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  • 收稿日期:  2023-01-10
  • 修回日期:  2023-04-25
  • 网络出版日期:  2023-08-31
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