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The ultra efficiency of energy transfer in photosynthesis has important biological significance. The underlying mechanism of energy transfer has never stopped being explored. Possible roles of quantum mechanics behind the natural phenomenon lead to many explorations in the field. Yet conventional mechanisms based on Förster resonance energy transfer or localized quantum coherence effects face certain challenges in explaining the unusual efficiency. We hereby bring up the attention of the dual properties of wave and particle of quantum mechanics into this context. In a previous research, we attributed the success of a similar efficiency in an artificial photosynthesis experiment to a mechanism mediated by resonant confinement of exciton-polariton. This paper extends the work to biological photosynthesis in higher plants and green sulfur bacteria. We explore specifically whether the exciton-polaritons of light-harvesting pigments, constrained by the optical cavity resonance, can act as intermediate states to mediate energy transfer. Namely, the pigments give a full play to their dual roles, receiving sunlight in the form of particle-like excitons, and rapidly transferring them to the reaction centers in the form of wave-like polaritons for maximal energy utilization. Taking realistic structure and data into account and based on approximate theoretical models, our quantitative estimate shows that such a mechanism is indeed capable of explaining at least partly the efficiency of photosynthesis. With comprehensive discussion, many deficits in the theoretical modeling can be reasonably reduced. Thus the conclusion may be further strengthened by realistic situations. Meanwhile, the underlying approach may also be extended to e.g. photovoltaic applications and neural signal transmissions, offering similar mechanisms for other energy transfer processes.
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Keywords:
- photosynthesis /
- exciton-polariton /
- higher plants /
- green sulfur bacteria
[1] 林荣呈, 杨文强, 王柏臣, 于龙江, 王文达, 田利金, 迟伟, 卢庆陶, 韩广业, 匡廷云 2021 中国科学: 生命科学 51 1376
Google Scholar
Lin R C, Yang W Q, Wang B C, Yu L J, Wang W D, Tian L J, Chi W, Lu Q T, Hang G Y, Kuang T Y 2021 Sci. China Life. Sci. 51 1376
Google Scholar
[2] Mirkovic T, Ostroumov E E, Anna J M, van Grondelle R, Govindjee, Scholes G D 2016 Chem. Rev. 117 249
Google Scholar
[3] Chen Y C, Song B, Leggett A J, Ao P, Zhu X M 2019 Phys. Rev. Lett. 122 257402
Google Scholar
[4] Fassioli F, Dinshaw R, Arpin P C, Scholes G D 2014 J. R. Soc. Interface 11 20130901
Google Scholar
[5] Christensson N, Kauffmann H F, Pullerits T, Mančal T 2012 J. Phys. Chem. B 116 7449
Google Scholar
[6] Reimers J R, Biczysko M, Bruce D, et al. 2016 BBA-Biomembranes 1857 1627
Google Scholar
[7] Huang K 1951 Nature 167 779
Google Scholar
[8] Pines D, Bohm D 1952 Phys. Rev. 85 338565
Google Scholar
[9] Coles D, Flatten L C, Sydney T, Hounslow E, Saikin S K, Aspuru-Guzik A, Vedral V, Tang J K-H, Taylor R A, Smith J M, Lidzey D G 2017 Small 13 1701777
Google Scholar
[10] Coles D M, Yang Y S, Wang Y Y, Grant R T, Taylor R A, Saikin S K, Aspuru-Guzik A, Lidzey D G, Tang J K H, Smith J M 2014 Nat. Commun. 5 5561
Google Scholar
[11] Deng H, Weihs G, Santori C, Bloch J, Yamamoto Y 2002 Science 298 199
Google Scholar
[12] Kasprzak J, Richard M, Kundermann S, et al. 2006 Nature 443 409
Google Scholar
[13] Lerario G, Fieramosca A, Barachati F, Ballarini D, Daskalakis K S, Dominici L, De Giorgi M, Maier S A, Gigli G, Kéna-Cohen S, Sanvitto D 2017 Nat. Phys. 13 837
Google Scholar
[14] Chen P Z, Weng Y X, Niu L Y, Chen Y Z, Wu L Z, Tung C H, Yang Q Z 2016 Angew. Chem. Int. Edit. 55 2759
Google Scholar
[15] Strümpfer J, Sener M, Schulten K 2012 J. Phys. Chem. Lett. 3 536
Google Scholar
[16] 朱圣庚, 徐长法, 王镜岩, 张庭芳, 昌增益, 秦咏梅 2016 生物化学 (第四版)(北京: 高等教育出版社) 第175—196页
Zhu S G, Xu C F, Wang J Y, Zhang T F, Chang Z Y, Qin Y M 2016 Biochemistry (Fourth edition) (Beijing: Higher Education Press) pp175–196 (in Chinese)
[17] Staehelin L A 2003 Photosynth. Res. 76 185
Google Scholar
[18] Murray J W, Duncan J, Barber J 2006 Trends Plant Sci. 11 152
Google Scholar
[19] Overmann J 2001 Archaea and the Deeply Branching and Phototrophic Bacteria (Berlin: Springer) p601
[20] Wahlund T M, Woese C R, Castenholz R W, Madigan M T 1991 Arch. Microbiol 156 81
Google Scholar
[21] Oostergetel G T, van Amerongen H, Boekema E J 2010 Photosynth. Res. 104 245
Google Scholar
[22] Krasnok A E, Slobozhanyuk A P, Simovski C R, Tretyakov S A, Poddubny A N, Miroshnichenko A E, Kivshar Y S, Belov P A 2015 Sci. Rep. UK. 5 1
Google Scholar
[23] Mustárdy L, Buttle K, Steinbach G, Garab G 2008 The Plant Cell 20 2552
Google Scholar
[24] Kirchhoff H, Tremmel I, Haase W, Kubitscheck U 2004 Biochemistry-US 43 9204
Google Scholar
[25] Oviedo M B, Sanchez C G 2011 J. Phys. Chem. A 115 12280
Google Scholar
[26] Brüggemann B, Sznee K, Novoderezhkin V, van Grondelle R, May V 2004 J. Phys. Chem. B 108 13536
Google Scholar
[27] Kühlbrandt W, Wang D N 1991 Nature 350 130
Google Scholar
[28] Hankamer B, Barber J, Boekema E J 1997 Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 641
Google Scholar
[29] Nield J, Orlova E V, Morris E P, Gowen B, van Heel M, Barber J 2000 Nat. Struct. Biol. 7 44
Google Scholar
[30] Bassi R, Hyer-Hansen G, Barbato R, Giacometti G M, Simpson D J 1987 J. Biol. Chem. 262 13333
Google Scholar
[31] Mimuro M, Nozawa T, Tamai N, Shimada K, Yamazaki L, Lin S, Knox R S, Wittmershaus B P, Brune D C, Blankenship R E 1989 J. Phys. Chem. 93 7503
Google Scholar
[32] Orf G S, Blankenship R E 2013 Photosynth. Res. 116 315
Google Scholar
[33] Günther L M, Jendrny M, Bloemsma E A, Tank M, Oostergetel G T, Bryant D A, Knoester J, Kohler J 2016 J. Phys. Chem. B 120 5367
Google Scholar
[34] Lavergne J 2006 BBA-Biomembranes 1757 1453
Google Scholar
[35] Sahoo P C, Pant D, Kumar M, Puri S K, Ramakumar S S V 2020 Trends. Biotechnol. 38 1245
Google Scholar
[36] Song B, Shu Y S 2020 Nano Res. 13 38
Google Scholar
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图 3 矩形光腔中激子极化子介导能量示意图
Figure 3. Processes of exciton-polariton mediated energy transfer in a rectangular optical cavity.
图 4 当选定一组
$ {k_x} $ ,$ {k_y} $ 模式时, 红色曲线表示极化子的归一化能量$ {E_{\boldsymbol{k}}}/{E_1} $ 随$ {k_z}/{k_{\text{e}}} $ 的变化情况. 水平实线(顶边)和虚线分别表征$ {E_1} $ 和$ {E_2} $ , 竖直虚线右侧的部分表示全内反射所限制的模式 (a)${k_x} = {k_{\text{e}}}{, }\;{k_y} = {k_{\text{e}}}{, }\;{k_z} \geqslant 0.67{k_{\text{e}}};$ (b)${k_x} ={1}/{2}{k_{\text{e}}}{, }\;{k_y} = {k_{\text{e}}},$ ${k_z} \geqslant 1.1{k_{\text{e}}}$ Figure 4. The solid (red) curve shows the dependence of normalized energy
$ {E_{\boldsymbol{k}}}/{E_1} $ , on the quasi-continuous$ {k_z}/{k_{\text{e}}} $ for a selected set of$ {k_x} $ ,$ {k_y} $ .The horizontal solid line (top frame-border) and the horizontal dashed line represents$ {E_1} $ and$ {E_2} $ , the modes to the right of the vertical dash line are confined by total internal reflection: (a)${k_x} = {k_{\text{e}}}{, }~{k_y} = {k_{\text{e}}}{, }~{k_z} \geqslant 0.67{k_{\text{e}}}$ ; (b)${k_x} = {1}/{2}{k_{\text{e}}}{, }\;{k_y} = $ $ {k_{\text{e}}}{, }\;{k_z} \geqslant 1.1{k_{\text{e}}} $ .
图 5 当选定一组
$ {k_x} $ ,$ {k_y} $ 模式时, 红色曲线表示极化子的归一化能量$ {E_{\boldsymbol{k}}}/{E_1} $ 随$ {k_z}/{k_{\text{e}}} $ 的变化情况. 水平实线(顶边)和虚线分别表征$ {E_1} $ 和$ {E_2} $ , 竖直虚线右侧的部分表示全内反射所限制的模式 (a)$ {k_x} = {k_{\text{e}}}{, }~{k_y} = {k_{\text{e}}}{, }{k_z} \geqslant 0.67{k_{\text{e}}} $ ; (b)${k_x} = {1}/{2}{k_{\text{e}}}{, }~{k_y} = $ ${k_{\text{e}}}{, }~{k_z} \geqslant 1.1{k_{\text{e}}} $ Figure 5. The solid (red) curve shows the dependence of normalized energy
$ {E_{\boldsymbol{k}}}/{E_1} $ , on the quasi-continuous$ {k_z}/{k_{\text{e}}} $ for a selected set of$ {k_x} $ ,$ {k_y} $ . The horizontal solid line (top frame-border) and the horizontal dashed line represents$ {E_1} $ and$ {E_2} $ , the modes to the right of the vertical dash line are confined by total internal reflection: (a)$ {k_x} = {k_{\text{e}}}{, }~{k_y} = {k_{\text{e}}}{, }~{k_z} \geqslant 0.67{k_{\text{e}}} $ ; (b)${k_x} = {1}/{2}{k_{\text{e}}}{, }~{k_y} = $ $ {k_{\text{e}}}{, }~{k_z} \geqslant 1.1{k_{\text{e}}} $ .表 1 高等植物体的参数值
Table 1. Parameters of higher plants.
光合场所: 基粒 主要集光色素: Chl a 形状 直径 高度 吸收峰 发射峰 偶极矩 能量值 圆柱体 500 nm 250 nm 674 nm 683 nm 4.58 deb 14841 cm–1 
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表 2 绿色硫细菌的参数值
Table 2. Parameters of green sulfur bacteria.
光合场所: 绿色硫细菌 主要集光色素: BChl c 形状 直径 高度 吸收峰 发射峰 偶极矩 能量值 椭圆体 600 nm 1600 nm 740 nm 750 nm 5.19 deb 13476 cm–1
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[1] 林荣呈, 杨文强, 王柏臣, 于龙江, 王文达, 田利金, 迟伟, 卢庆陶, 韩广业, 匡廷云 2021 中国科学: 生命科学 51 1376
Google Scholar
Lin R C, Yang W Q, Wang B C, Yu L J, Wang W D, Tian L J, Chi W, Lu Q T, Hang G Y, Kuang T Y 2021 Sci. China Life. Sci. 51 1376
Google Scholar
[2] Mirkovic T, Ostroumov E E, Anna J M, van Grondelle R, Govindjee, Scholes G D 2016 Chem. Rev. 117 249
Google Scholar
[3] Chen Y C, Song B, Leggett A J, Ao P, Zhu X M 2019 Phys. Rev. Lett. 122 257402
Google Scholar
[4] Fassioli F, Dinshaw R, Arpin P C, Scholes G D 2014 J. R. Soc. Interface 11 20130901
Google Scholar
[5] Christensson N, Kauffmann H F, Pullerits T, Mančal T 2012 J. Phys. Chem. B 116 7449
Google Scholar
[6] Reimers J R, Biczysko M, Bruce D, et al. 2016 BBA-Biomembranes 1857 1627
Google Scholar
[7] Huang K 1951 Nature 167 779
Google Scholar
[8] Pines D, Bohm D 1952 Phys. Rev. 85 338565
Google Scholar
[9] Coles D, Flatten L C, Sydney T, Hounslow E, Saikin S K, Aspuru-Guzik A, Vedral V, Tang J K-H, Taylor R A, Smith J M, Lidzey D G 2017 Small 13 1701777
Google Scholar
[10] Coles D M, Yang Y S, Wang Y Y, Grant R T, Taylor R A, Saikin S K, Aspuru-Guzik A, Lidzey D G, Tang J K H, Smith J M 2014 Nat. Commun. 5 5561
Google Scholar
[11] Deng H, Weihs G, Santori C, Bloch J, Yamamoto Y 2002 Science 298 199
Google Scholar
[12] Kasprzak J, Richard M, Kundermann S, et al. 2006 Nature 443 409
Google Scholar
[13] Lerario G, Fieramosca A, Barachati F, Ballarini D, Daskalakis K S, Dominici L, De Giorgi M, Maier S A, Gigli G, Kéna-Cohen S, Sanvitto D 2017 Nat. Phys. 13 837
Google Scholar
[14] Chen P Z, Weng Y X, Niu L Y, Chen Y Z, Wu L Z, Tung C H, Yang Q Z 2016 Angew. Chem. Int. Edit. 55 2759
Google Scholar
[15] Strümpfer J, Sener M, Schulten K 2012 J. Phys. Chem. Lett. 3 536
Google Scholar
[16] 朱圣庚, 徐长法, 王镜岩, 张庭芳, 昌增益, 秦咏梅 2016 生物化学 (第四版)(北京: 高等教育出版社) 第175—196页
Zhu S G, Xu C F, Wang J Y, Zhang T F, Chang Z Y, Qin Y M 2016 Biochemistry (Fourth edition) (Beijing: Higher Education Press) pp175–196 (in Chinese)
[17] Staehelin L A 2003 Photosynth. Res. 76 185
Google Scholar
[18] Murray J W, Duncan J, Barber J 2006 Trends Plant Sci. 11 152
Google Scholar
[19] Overmann J 2001 Archaea and the Deeply Branching and Phototrophic Bacteria (Berlin: Springer) p601
[20] Wahlund T M, Woese C R, Castenholz R W, Madigan M T 1991 Arch. Microbiol 156 81
Google Scholar
[21] Oostergetel G T, van Amerongen H, Boekema E J 2010 Photosynth. Res. 104 245
Google Scholar
[22] Krasnok A E, Slobozhanyuk A P, Simovski C R, Tretyakov S A, Poddubny A N, Miroshnichenko A E, Kivshar Y S, Belov P A 2015 Sci. Rep. UK. 5 1
Google Scholar
[23] Mustárdy L, Buttle K, Steinbach G, Garab G 2008 The Plant Cell 20 2552
Google Scholar
[24] Kirchhoff H, Tremmel I, Haase W, Kubitscheck U 2004 Biochemistry-US 43 9204
Google Scholar
[25] Oviedo M B, Sanchez C G 2011 J. Phys. Chem. A 115 12280
Google Scholar
[26] Brüggemann B, Sznee K, Novoderezhkin V, van Grondelle R, May V 2004 J. Phys. Chem. B 108 13536
Google Scholar
[27] Kühlbrandt W, Wang D N 1991 Nature 350 130
Google Scholar
[28] Hankamer B, Barber J, Boekema E J 1997 Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 641
Google Scholar
[29] Nield J, Orlova E V, Morris E P, Gowen B, van Heel M, Barber J 2000 Nat. Struct. Biol. 7 44
Google Scholar
[30] Bassi R, Hyer-Hansen G, Barbato R, Giacometti G M, Simpson D J 1987 J. Biol. Chem. 262 13333
Google Scholar
[31] Mimuro M, Nozawa T, Tamai N, Shimada K, Yamazaki L, Lin S, Knox R S, Wittmershaus B P, Brune D C, Blankenship R E 1989 J. Phys. Chem. 93 7503
Google Scholar
[32] Orf G S, Blankenship R E 2013 Photosynth. Res. 116 315
Google Scholar
[33] Günther L M, Jendrny M, Bloemsma E A, Tank M, Oostergetel G T, Bryant D A, Knoester J, Kohler J 2016 J. Phys. Chem. B 120 5367
Google Scholar
[34] Lavergne J 2006 BBA-Biomembranes 1757 1453
Google Scholar
[35] Sahoo P C, Pant D, Kumar M, Puri S K, Ramakumar S S V 2020 Trends. Biotechnol. 38 1245
Google Scholar
[36] Song B, Shu Y S 2020 Nano Res. 13 38
Google Scholar
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