Impact of energy limitations on function and resilience in long-wavelength Photosystem II.
Impact of energy limitations on function and resilience in long-wavelength Photosystem II.
复制标题
能量限制对长波长光系统II功能及恢复能力的影响
DOI：
10.7554/elife.79890
复制
发表时间：
2022-07-19
期刊：
影响因子：
7.7
通讯作者：
Rutherford, A. William
中科院分区：
文献类型：
--
作者：
Viola, Stefania;Roseby, William;Santabarbara, Stefano;Nurnberg, Dennis;Assuncao, Ricardo;Dau, Holger;Selles, Julien;Boussac, Alain;Fantuzzi, Andrea;Rutherford, A. William
光系统II（PSII）利用红光的能量来分解水并还原醌，这是一个基于叶绿素a（Chl - a）光化学的耗能过程。两种类型的蓝藻光系统II能够利用叶绿素d（Chl - d）和叶绿素f（Chl - f），借助能量较低的远红光来进行相同的反应。滨海红藻（Acaryochloris marina）的光系统II中，35个叶绿素a除一个之外全部被叶绿素d取代，而兼性远红光物种嗜热聚球藻（Chroococcidiopsis thermalis）的光系统II仅有4个叶绿素f、1个叶绿素d和30个叶绿素a。从生物能量学角度考虑，预计远红光光系统II会损失光化学效率和/或对光损伤的恢复能力。在此，我们比较了叶绿素f - 光系统II、叶绿素d - 光系统II和叶绿素a - 光系统II的酶周转效率、正向电子转移、逆向反应及光损伤情况。我们发现：（i）所有类型的光系统II在酶周转方面效率相当；（ii）与叶绿素a - 光系统II和叶绿素f - 光系统II相比，叶绿素d - 光系统II受体侧经修饰的能隙有利于通过PD1⁺Phe⁻再填充进行复合，从而导致单线态氧生成增加，对高光损伤更为敏感；（iii）叶绿素f - 光系统II受体侧的能隙经过调整，可避免有害的逆向反应，相较于光能利用效率，更有利于对光损伤的恢复能力。这些结果可通过电子转移辅因子Phe和QA的氧化还原调节差异，以及与原初电子供体共享激发能的叶绿素数量和布局差异来解释。光系统II以两种不同方式适应了较低能量，每种方式都适合其特定环境，但存在不同的功能代价。
藻类、植物和蓝藻进行一种称为光合作用的过程，在此过程中，二氧化碳和水转化为氧气和富含能量的碳化合物。该过程的第一步涉及一种名为光系统II的酶，它利用光能从水中提取电子，以帮助捕获二氧化碳。
如果光系统吸收过多的光，就会产生大量被称为活性氧的化合物，这些化合物会损伤光系统并杀死细胞。为确保光系统高效运作并保护其免受损伤，吸收光的能量约有一半以热的形式耗散，其余能量则储存于光合作用产物中。
标准形式的光系统II利用可见光的能量，但一些蓝藻含有不同类型的光系统II，它们利用能量较低的远红光进行相同的化学反应。一种远红光光系统II存在于滨海红藻中，这是一种生活在稳定远红光环境且避开可见光的蓝藻。另一种存在于嗜热聚球藻中，这种蓝藻在避开可见光时可使用其远红光光系统II，而暴露于可见光下时则可切换为使用标准光系统II。由于能够利用较少能量工作，这两种远红光光系统II似乎比标准光系统II更高效，但尚不清楚这种特性是否存在任何弊端。
维奥拉（Viola）等人通过测量这些酶的效率、产生的活性氧数量以及由此导致的光诱导损伤，将标准光系统II与嗜热聚球藻和滨海红藻的远红光光系统II类型进行了比较。实验表明，滨海红藻的远红光光系统II效率很高，但在高光条件下会产生较高水平的活性氧。另一方面，嗜热聚球藻的远红光光系统II在收集和利用远红光方面效率较低，但更具稳健性，产生的活性氧较少。
尽管存在这些权衡，但对能够利用远红光光合作用的农作物或藻类进行工程改造，可能有助于提高粮食和生物质产量。更好地理解这两种远红光光系统II在效率与恢复能力之间的权衡，有助于确定哪些特性有益以及在何种条件下有益。这项研究也增进了我们对标准光系统II如何平衡光吸收和损伤限制，从而在多变环境中高效运作的认识。
Photosystem II (PSII) uses the energy from red light to split water and reduce quinone, an energy-demanding process based on chlorophyll a (Chl-a) photochemistry. Two types of cyanobacterial PSII can use chlorophyll d (Chl-d) and chlorophyll f (Chl-f) to perform the same reactions using lower energy, far-red light. PSII from Acaryochloris marina has Chl-d replacing all but one of its 35 Chl-a, while PSII from Chroococcidiopsis thermalis, a facultative far-red species, has just 4 Chl-f and 1 Chl-d and 30 Chl-a. From bioenergetic considerations, the far-red PSII were predicted to lose photochemical efficiency and/or resilience to photodamage. Here, we compare enzyme turnover efficiency, forward electron transfer, back-reactions and photodamage in Chl-f-PSII, Chl-d-PSII, and Chl-a-PSII. We show that: (i) all types of PSII have a comparable efficiency in enzyme turnover; (ii) the modified energy gaps on the acceptor side of Chl-d-PSII favour recombination via PD1+Phe- repopulation, leading to increased singlet oxygen production and greater sensitivity to high-light damage compared to Chl-a-PSII and Chl-f-PSII; (iii) the acceptor-side energy gaps in Chl-f-PSII are tuned to avoid harmful back reactions, favouring resilience to photodamage over efficiency of light usage. The results are explained by the differences in the redox tuning of the electron transfer cofactors Phe and QA and in the number and layout of the chlorophylls that share the excitation energy with the primary electron donor. PSII has adapted to lower energy in two distinct ways, each appropriate for its specific environment but with different functional penalties. Algae, plants and cyanobacteria perform a process called photosynthesis, in which carbon dioxide and water are converted into oxygen and energy-rich carbon compounds. The first step of this process involves an enzyme called photosystem II, which uses light energy to extract electrons from water to help capture the carbon dioxide. If the photosystem absorbs too much light, compounds known as reactive oxygen species are produced in quantities that damage the photosystem and kill the cell. To ensure that the photosystem works efficiently and to protect it from damage, about half of the energy from the absorbed light is dissipated as heat, while the rest of the energy is stored in the products of photosynthesis. The standard form of photosystem II uses the energy of visible light, but some cyanobacteria contain different types of photosystem II, which do the same chemical reactions using lower energy far-red light. One type of far-red photosystem II is found in Acaryochloris marina, a cyanobacterium living in stable levels of far-red light, shaded from visible light. The other type is found in a cyanobacterium called Chroococcidiopsis thermalis, which can switch between using its far-red photosystem II when shaded from visible light and using its standard photosystem II when exposed to it. Being able to work with less energy, the two types of far-red photosystem II appear to be more efficient than the standard one, but it has been unclear if there were any downsides to this trait. Viola et al. compared the standard photosystem II with the far-red photosystem II types from C. thermalis and A. marina by measuring the efficiency of these enzymes, the quantity of reactive oxygen species produced, and the resulting light-induced damage. The experiments revealed that the far-red photosystem II of A. marina is highly efficient but produces elevated levels of reactive oxygen species if exposed to high light conditions. On the other hand, the far-red photosystem II of C. thermalis is less efficient in collecting and using far-red light, but is more robust, producing fewer reactive oxygen species. Despite these tradeoffs, engineering crop plants or algae that could use far-red photosynthesis may help boost food and biomass production. A better understanding of the trade-offs between efficiency and resilience in the two types of far-red photosystem II could determine which features would be beneficial, and under what conditions. This work also improves our knowledge of how the standard photosystem II balances light absorption and damage limitation to work efficiently in a variable environment.