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.
Keywords: cyanobacteria; molecular biophysics; photochemistry; photosystem II; structural biology.
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.
© 2022, Viola et al.