光系统II光驱动CO2同化的光合作用

doi:10.1016/S1872-2067(22)64170-6

催化学报 ›› 2023, Vol. 44: 117-126.DOI: 10.1016/S1872-2067(22)64170-6

光系统II光驱动CO₂同化的光合作用

李跃辉^a^,¹, 司端惠^a^,¹, 王旺银^b^,^*(), 薛松^c, 商文喆^a, 迟占有^c, 李灿^b, 郝策^a^,^*(), Govindjee Govindjee^d, 史彦涛^a^,^*()

^a大连理工大学化工学院化学系, 智能材料化工前沿科学中心, 精细化工国家重点实验室, 辽宁大连 116024, 中国
^b中国科学院大连化学物理研究所, 催化基础国家重点实验室, 洁净能源国家实验室(筹), 辽宁大连 116023, 中国
^c大连理工大学生物工程学院, 辽宁大连 116023, 中国
^d伊利诺伊大学厄巴纳香槟分校, 生物化学系, 植物生物学系和生物物理学与定量生物学中心, 伊利诺伊州, 美国

收稿日期:2022-07-10 接受日期:2022-09-18 出版日期:2023-01-18 发布日期:2022-12-08
通讯作者: 王旺银,郝策,史彦涛
作者简介:¹共同第一作者.
基金资助:
国家自然科学基金(51773025);国家自然科学基金(21677029);国家自然科学基金(22088102);辽宁省兴辽英才青年拔尖人才项目(XLYC2007038);辽宁省兴辽英才青年拔尖人才项目(XLYC2008032);中央高校基础研究经费(DUT22LAB602)

Light-driven CO₂ assimilation by photosystem II and its relation to photosynthesis

Yuehui Li^a^,¹, Duanhui Si^a^,¹, Wangyin Wang^b^,^*(), Song Xue^c, Wenzhe Shang^a, Zhanyou Chi^c, Can Li^b, Ce Hao^a^,^*(), Govindjee Govindjee^d, Yantao Shi^a^,^*()

^aState Key laboratory of Fine Chemicals, Frontier Science Center for Smart Materials, Department of Chemistry, School of Chemical Engineering, Dalian University of Technology, Dalian 116024, Liaoning, China
^bState Key Laboratory of Catalysis, Dalian National Laboratory for Clean Energy, Dalian Institute of Chemical Physics, Chinese Academy of Sciences, Dalian 116023, Liaoning, China
^cSchool of Bioengineering, Dalian University of Technology, Dalian 116024, Liaoning, China
^dDepartment of Biochemistry, Department of Plant Biology and Center of Biophysics& Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana 61801, USA

Received:2022-07-10 Accepted:2022-09-18 Online:2023-01-18 Published:2022-12-08
Contact: Wangyin Wang, Ce Hao, Yantao Shi
About author:¹ Contributed equally to this work.
Supported by:
National Natural Science Foundation of China(51773025);National Natural Science Foundation of China(21677029);National Natural Science Foundation of China(22088102);LiaoNing Revitalization Talents Program(XLYC2007038);LiaoNing Revitalization Talents Program(XLYC2008032);Fundamental Research Funds for the Central Universities(DUT22LAB602)

摘要/Abstract

摘要：

光合作用作为地球上最重要的化学反应, 是一切生命活动赖以生存的基础. 光合作用分为光反应和暗反应两个阶段. 通常认为, 光反应阶段产生O₂, 暗反应阶段CO₂被还原(也称“CO₂同化”). 尽管这一观点已被公众所熟知, 但也存在诸多疑点, 一些科学家(包括1931年的诺贝尔生理学或医学奖得主Otto Warburg)认为, CO₂也可能在光反应阶段作为反应底物参与了产氧并被还原. 然而, 该观点至今没有在实验上获得充足的证据支持. 那么, 在光反应阶段是否能够进行CO₂同化?如果能够发生, 产物和机理是什么?毫无疑问, 这些科学问题具有十分重要的研究价值, 对这些问题的探索能帮助我们更加充分认识光合作用机制. 然而, 自上世纪十年代以来, 相关研究已陷入停滞状态.

为了解开光合作用领域的这个重要科学谜团, 即在光合作用中CO₂是否能通过光反应被还原, 本文选取三类不同层次的光合作用体系(小球藻、叶绿体、PSII中心复合体)为研究对象, 结合原位质谱、气相色谱和同位素标记等手段, 设计了一系列实验, 排除了呼吸作用和其它因素干扰, 实验发现在光反应阶段PSII中心复合体不但产生O₂, 还能产生C1化合物CH₃OH. ¹³CO₂和C¹⁸O₂标记实验结果表明, CH₃OH来源于CO₂光还原, 排除了CH₃OH来自于光呼吸或细胞壁果胶脱甲基分解的可能. 说明光合作用光反应阶段能够进行CO₂还原, 反应场所是PSII中心复合体, 这与CO₂的同化只能发生在暗反应阶段的传统观点相矛盾. 因此, 除了非光依赖性CO₂同化这一已知路径外, 还有一条未知的光驱动CO₂同化路径. 进一步推测, 这种CO₂光还原路径可能与暗反应下的CO₂同化同时进行. 目前, 对这种光驱动下CO₂同化机制仍需进一步深入研究. 综上, 本文丰富了人们对光合作用机理以及CO₂同化路径的认知, 并为长期以来存在争议的CH₃OH来源问题提供了新解释.

关键词: 光合作用, PSII中心复合体, 光反应, CO₂同化, 甲醇

Abstract:

For natural oxygenic photosynthesis, there is a consensus that H₂O is oxidized to molecular oxygen by photosystem II (PSII) in the grana, while CO₂ assimilation takes place, long after oxygen evolution, in light-independent reactions, for example, through the Calvin-Benson Cycle in the stroma. Here, we report, for the first time, light-driven CO₂ assimilation by the PSII core complex, where the formation of methanol, along with the oxygen evolution, is validated by in-situ mass spectrometry, gas chromatography and isotopic labeling experiments. Such an unusual CO₂ assimilation is likely to be a simultaneous event along with the usual electron transfer occurring in normal light-independent assimilation. This discovery is extraordinary and is of great significance as it may substantially modify our understanding of the mechanism of photosynthesis.

Key words: Photosynthesis, Photosystem II core complex, Photoreaction, CO₂ assimilation, Methanol

李跃辉, 司端惠, 王旺银, 薛松, 商文喆, 迟占有, 李灿, 郝策, Govindjee Govindjee, 史彦涛. 光系统II光驱动CO₂同化的光合作用[J]. 催化学报, 2023, 44: 117-126.

Yuehui Li, Duanhui Si, Wangyin Wang, Song Xue, Wenzhe Shang, Zhanyou Chi, Can Li, Ce Hao, Govindjee Govindjee, Yantao Shi. Light-driven CO₂ assimilation by photosystem II and its relation to photosynthesis[J]. Chinese Journal of Catalysis, 2023, 44: 117-126.

×
扫码分享

导出引用管理器 EndNote|Ris|BibTeX

链接本文: https://www.cjcatal.com/CN/10.1016/S1872-2067(22)64170-6

https://www.cjcatal.com/CN/Y2023/V44/I1/117

图/表 4

Fig. 1. The measurements of the production of O2 and CH3OH by the green alga Chlorella and chloroplasts, isolated from spinach leaves, upon light illumination. (a,b) A diagram of Chlorella cells and spinach chloroplasts. (c,d) The O2 and CH3OH detected by in-situ real-time MS in Chlorella and spinach suspensions. (e,f) The CH3OH detected by GC in Chlorella cells and in spinach chloroplasts. The blank experiments E and F refer to those carried out in the dark.

Fig. 2. The labeled CH3OH detected by in-situ RT-MS in Chlorella cells and spinach chloroplasts upon light illumination. (a,b) The 13CH3OH (m/z = 33) detected by RT-MS for Chlorella and spinach chloroplasts labeled with 13CO2. (c,d) The CH318OH (m/z = 33) detected by RT-MS for Chlorella and spinach chloroplasts, labeled with C18O2.

Fig. 3. The measurements of the production of O2 and CH3OH by the PSII core complex upon light illumination. (a) The O2 and CH3OH detected by in-situ RT-MS. (b) The CH3OH detected by GC; The O2 (c) and CH3OH (d) relative amounts detected by RT-MS under different concentration of CO2 in carrier gas (0, 88, 220, 1175, 10000, 15000 ppm). The 13CH3OH (e) and CH318OH (f) detected by in-situ RT-MS in 13CO2 and C18O2 labeling experiments.

Fig. 4. The O2 (a) and CH3OH (b) detected by RT-MS for the PSII core complex, upon light illumination, involving different electron accepters. (c) A schematic depiction of the electron flow across the three protein complexes, as well as the light-driven CO2 light assimilation possibly occurring prior to QA.

参考文献

[1]	R. E. Blankenship, Molecular Mechanisms of Photosynthesis, 3^rdEdition, Wiley, 2021, 1-9.
[2]	D. Shevela, L. O. Björn, Govindjee, Photosynthesis: Solar Energy for Life, World Scientific, 2018, 1.
[3]	M. P. Johnson, Essays Biochem., 2016, 60, 255-273.
[4]	D. Shevela, J. J. Eaton-Rye, J. R. Shen, Govindjee, Biochim. Biophys. Acta-Bioenerg., 2012, 1817, 1134-1151.
[5]	D. J. Blubaugh, Govindjee. Biochim. Biophys. Acta-Bioenerg., 1988, 936, 208-214.
[6]	D. J. Blubaugh, Govindjee. Photosynth. Res., 1988, 19, 85-128.
[7]	R. Hienerwadel, C. Berthomieu, Biochemistry, 1995, 34, 16288-16297.
[8]	Y. Umena, K. Kawakami, J. R. Shen, N. Kamiya, Nature, 2011, 473, 55-60.
[9]	V. V. Klimov, S. V. Baranov, Bicarbonate requirement for the water-oxidizing complex of Photosystem II. Biochim. Biophys. Acta-Bioenerg., 2001, 1503, 187-196.
[10]	A. Stemler, Biochim. Biophys. Acta-Bioenerg., 1980, 593, 103-112.
[11]	P. A. Castelfranco, Y. K. Lu, A. J. stemler, Photosynth. Res., 2007, 94, 235-246.
[12]	V. V. Klimov, S. I. Allakhverdiev, S. V. Baranov, Y. M. Feyziev, Photosynth. Res., 1995, 46, 219-225.
[13]	V. V. Klimov, S. I. Allakhverdiev, Y. M. Feyziev, S. V. Baranov, FEBS Lett., 1995, 363, 251-255.
[14]	S. I. Allakhverdiev, I. Yruela, R. Picorel, V. V. Klimov, Proc. Natl. Acad. Sci. U. S. A., 1997, 94, 5050-5054.
[15]	R. J. Hulsebosch, S. I. Allakhverdiev, V. V. Klimov, R. Picorel, A. J. Hoff, FEBS Lett., 1998, 424, 146-148.
[16]	G. Ananyev, G. C. Dismukes. Photosynth. Res., 2005, 84, 355-365.
[17]	T. Shutova, H. Kenneweg, J. Buchta, J. Nikitina, V. Terentyev, S. Chernyshov, B. Andersson, S. I. Allakhverdiev, V. V. Klimov, H. Dau, W. Junge, G. Samuelsson, EMBO J., 2008, 27, 782-791.
[18]	R. Y. Stanier, R. Kunisawa, M. Mandel, Bacteriological reviews, 1971, 35, 171-205.
[19]	H. K. Lichtenthaler, Methods Enzymol., 1987, 148, 350-382.
[20]	D. A. Berthold, G. T. Babcock, C. F. Yocum, FEBS Letters, 1981, 134, 231-234.
[21]	K. Nakazato, C. Toyoshima, I. Enami, Y. Inoue, J. Mol. Biol., 1996, 257, 225-232.
[22]	W. Wang, J. Chen, C. Li, W. Tian, Nat. Commun., 2014, 5, 4647.
[23]	M. Nemecek-Marshall, R. C. MacDonald, J. J. Franzen, C. L. Wojciechowski, R. Fall, Plant Physiol., 1995, 108, 1359-1368.
[24]	R. MacDonald, R. Fall, Atmos. Environ., 1993, 28, 1709-1713.
[25]	R. Fall, A. A. Benson, Trends Plant Sci., 1996, 1, 296-301.
[26]	Y. L. Dorokhov, E. V. Sheshukova, T. V. Komarova, Front. Plant Sci., 2018, 9, 1623.
[27]	C. Frenkel, J. S. Peters, D. M. Tieman, M. E. Tiznado, A. K. Handa, J. Biolog. Chem., 1998, 273, 4293-4295.
[28]	G. Govindjee, D. Shevela, L. O. Björn, Photosynth. Res., 2017, 133, 5-15.
[29]	M. J. West-Eberhard, J. A. C. Smith, K. Winter, Science, 2011, 332, 311-312.
[30]	M. Calvin, A. A. Benson, Science, 1948, 107, 476-480.
[31]	M. D. Hatch, C. R. Slack, Biochem. J., 1966, 101, 103-111.
[32]	K. Winter, J. A. C. Smith, Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution, Springer-Verlag, Berlin, 1996, 1.
[33]	M. Yao, Y. Liu, L. Fei, Y. Zhou, F. Wang, J. Chen, J. Phys. Chem. B, 2018, 122, 10478-10489.
[34]	D. J. Vinyard, G. M. Ananyev, G. C. Dismukes, Annu. Rev. Biochem., 2013, 82, 577-606.
[35]	H. Dau, I. Zaharieva, Acc. Chem. Res., 2009, 42, 1861-1870.
[36]	A. M. Nonomura, A. A. Benson, Proc. Natl. Acad. Sci. U. S. A., 1992, 89, 9794-9798.
[37]	R. N. Rowe, D. J. Farr, B. A. J. Richards, New Zealand J. Crop Horticul. Sci., 1994, 22, 335-337.
[38]	R. M. Devlin, P. C. Bhowmik, S. J. Karczmarczyk, PGRSA Quart., 1994, 22, 102-108.
[39]	L. Panella, J. N. Nishio, S. S. Martin, J. Sugarbeet Res., 2000, 37, 55-72.
[40]	R. Willstätter, A. Stoll, Untersuchungen über die Assimilation der Kohlensäure, Springer-Verlag. Berlin, 1918.
[41]	J. Franck, K. F. Herzfeld, J. Phys. Chem., 1941, 45, 978-1025.
[42]	O. Warburg, Annu. Rev. Biochem., 1964, 33, 1-14.
[43]	Y. Wu, Acta Geochim., 2021, 40, 650-658.
[44]	E. Gout, S. Aubert, R. Bligny, F. Rebeille, A. R. Nonomura, A. A. Benson, R. Douce, Plant Physiology, 2000, 123, 287-296.

光系统II光驱动CO₂同化的光合作用

Light-driven CO₂ assimilation by photosystem II and its relation to photosynthesis

RichHTML

PDF

Supporting Information

可视化

摘要/Abstract

引用本文

使用本文

扫码分享

图/表 4

参考文献

相关文章 15

编辑推荐

Metrics

[1]	石靖, 郭煜华, 谢飞, 章名田, 张洪涛. 氧化还原活性配体的电子效应对钌催化水氧化反应的影响[J]. 催化学报, 2023, 52(9): 271-279.
[2]	孙丽娟, 于晓慧, 唐丽永, 王伟康, 刘芹芹. 构建K₃PW₁₂O₄₀/CdS核壳S型异质结实现同步太阳能光催化分解水和选择性苯甲醇氧化反应[J]. 催化学报, 2023, 52(9): 164-175.
[3]	乔蔚, 于立策, 常进法, 杨甫林, 冯立纲. MoSe₂纳米片耦合Pt纳米颗粒用于高效双功能催化甲醇辅助水电解制氢[J]. 催化学报, 2023, 51(8): 113-123.
[4]	程璐, 陈许宁, 胡培君, 曹宵鸣. 双氧水对于单核铜分子筛催化甲烷直接氧化制甲醇反应性能的利弊[J]. 催化学报, 2023, 51(8): 135-144.
[5]	孙利娟, 王伟康, 路平, 刘芹芹, 王乐乐, 唐华. 纳米高熵合金实现光催化剂肖特基势垒的调控用于光催化制氢与苯甲醇氧化耦合反应[J]. 催化学报, 2023, 51(8): 90-100.
[6]	Mengistu Tulu Gonfa, 申升, 陈浪, 胡彪, 周威, 白张君, 区泽堂, 尹双凤. 光催化苯制苯酚的研究进展[J]. 催化学报, 2023, 49(6): 16-41.
[7]	刘润泽, 邵雪, 王畅, 戴卫理, 关乃佳. 甲醇制烃反应机理: 基础及应用研究[J]. 催化学报, 2023, 47(4): 67-92.
[8]	禹伟, 高教琪, 姚伦, 周雍进. 多形汉逊酵母细胞工厂实现甲醇生物转化合成3-羟基丙酸[J]. 催化学报, 2023, 46(3): 84-90.
[9]	林杉帆, 郅玉春, 张文娜, 袁小帅, 张成伟, 叶茂, 徐舒涛, 魏迎旭, 刘中民. 氢转移反应对分子筛催化甲醇和二甲醚动态自催化反应历程的贡献: 深入理解甲醛的生成机理和作用机制[J]. 催化学报, 2023, 46(3): 11-27.
[10]	沙峰, 唐珊, 汤驰洲, 冯振东, 王集杰, 李灿. ZnZrO_x固溶体催化剂表面羟基在CO₂加氢制甲醇中的作用[J]. 催化学报, 2023, 45(2): 162-173.
[11]	孟翔宇, 李睿, 杨峻懿, 许世明, 张辰晨, 尤可嘉, 马宝春, 管红霞, 丁勇. 六核环状钴配合物用于光催化CO₂到CO转化[J]. 催化学报, 2022, 43(9): 2414-2424.
[12]	王冶, 韩晶峰, 王男, 李冰, 杨淼, 吴一墨, 江子潇, 魏迎旭, 田鹏, 刘中民. SAPO-14催化的甲醇制丙烯反应: 反应机理与失活[J]. 催化学报, 2022, 43(8): 2259-2269.
[13]	Chuncheng Liu, Evgeny A. Uslamin, Sophie H. van Vreeswijk, Irina Yarulina, Swapna Ganapathy, Bert M. Weckhuysen, Freek Kapteijn, Evgeny A. Pidko. MFI/MEL分子筛催化甲醇制烯烃反应关键参数的集成方法[J]. 催化学报, 2022, 43(7): 1879-1893.
[14]	李垒, 欧阳汶俊, 郑泽锋, 叶凯航, 郭禹希, 秦延林, 伍珍珍, 林展, 王铁军, 张山青. 基于Pt@TiO₂催化剂光-热协同催化甲醇-水液相重整甲醇制氢[J]. 催化学报, 2022, 43(5): 1258-1266.
[15]	王旺银. 从液态阳光人工光合成淀粉[J]. 催化学报, 2022, 43(4): 895-897.