The Effect of Chilling on the Photosynthetic Apparatus of Microalga Lobosphaera incisa IPPAS C-2047

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Vasily V. Ptushenko^1,2,a*, Grigorii N. Bondarenko³, Elizaveta N. Vinogradova^4,5, Elena S. Glagoleva⁴, Olga V. Karpova⁴, Oxana S. Ptushenko⁴, Alexei E. Solovchenko⁴, Boris V. Trubitsin⁶, Olga B. Chivkunova⁴, Karina A. Shibzukhova⁴, and Pavel N. Shcherbakov⁴

¹Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119992 Moscow, Russia

²Emanuel Institute of Biochemical Physics, Russian Academy of Sciences, 119334 Moscow, Russia

³Faculty of Chemistry, Lomonosov Moscow State University, 119991 Moscow, Russia

⁴Faculty of Biology, Lomonosov Moscow State University, 119991 Moscow, Russia

⁵National Research Center “Kurchatov Institute”, 123182 Moscow Russia

⁶Faculty of Physics, Lomonosov Moscow State University, 119991 Moscow, Russia

^* To whom correspondence should be addressed.

Received September 25, 2021; Revised November 4, 2021; Accepted November 10, 2021

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Photosynthetic organisms have developed a set of mechanisms aimed at preventing photo-oxidative reactions in the photosynthetic apparatus (PSA) initiated by excessively absorbed light energy. Along with high irradiance, other stressors, e.g., chilling temperatures, can lead to the absorption of the excess of light energy and hence to photo-oxidative stress. Here, we studied induction of photoprotective mechanisms in response to chilling (0°C) at a low irradiance (50 µmol PAR photons m^–2·s^–1) in the cells of microalga Lobosphaera incisa IPPAS C-2047. After 4 days of incubation at a low temperature, L. incisa IPPAS C-2047 cells showed a notable decrease in the photochemical activity of photosystem II (PSII) and in the efficiency of photosynthetic electron transport, as well as a significant increase in the thermal dissipation of the absorbed light energy in the light-harvesting antenna. In contrast, most conventional markers of PSA acclimation to excess light energy [total chlorophyll and carotenoid content; violaxanthin cycle pigment content and de-epoxidation state; photosynthetic antenna, PSII, and photosystem I (PSI) ratio] remained virtually unchanged. The content of major unsaturated fatty acids also remained almost unaffected, except for arachidonic acid (increased by 40%) recently assumed to activate violaxanthin de-epoxidase by adjusting its lipid microenvironment. Significant changes (4-7-fold increase) were observed in the expression of the gene encoding protective protein LhcSR. Pre-conditioning at 5°C prior to the acclimation to 0°C augmented the PSA photochemical activity. Our data show that the mid-term (4-d) acclimation of L. incisa IPPAS C-2047 to a chilling temperature at a low irradiance triggers the PSA response resembling, in part, the response to high light but relying mostly on the LhcSR protein-dependent quenching of excitation in the photosynthetic antenna.

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KEY WORDS: high light stress, low temperature acclimation, fatty acid desaturation, arachidonic acid, thermal dissipation of light energy, LhcSR, microalgae

DOI: 10.1134/S0006297921120087

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