A desert Chlorella sp. that thrives at extreme high‐light intensities using a unique photoinhibition protection mechanism

Abstract

While light is the driving force of photosynthesis, excessive light can be harmful. Photoinhibition is one of the key processes that limit photosynthetic productivity. A well-defined mechanism that protects from photoinhibition has been described. Chlorella ohadii is a green micro-alga, isolated from biological desert soil crusts, which thrives under extreme high light (HL). Here, we show that this alga evolved unique protection mechanisms distinct from those of the green alga Chlamydomonas reinhardtii or plants. When grown under extreme HL, a drastic reduction in the size of light harvesting antennae occurs, resulting in the presence of core photosystem II, devoid of outer and inner antennas. This is accompanied by a massive accumulation of protective carotenoids and proteins that scavenge harmful radicals. At the same time, several elements central to photoinhibition protection in C. reinhardtii, such as psbS, light harvesting complex stress-related, photosystem II protein phosphorylation and state transitions are entirely absent or were barely detected. In addition, a carotenoid biosynthesis-related protein accumulates in the thylakoid membranes of HL cells and may function in sensing HL and protecting the cell from photoinhibition. Taken together, a unique photoinhibition protection mechanism evolved in C. ohadii, enabling the species to thrive under extreme-light intensities where other photosynthetic organisms fail to survive.

The protein phosphorylation landscape in photosystem I of the desert algae Chlorella sp.

“…Each phosphorylated peptide was found in only one of the two methods and there was no peptide found in both. The grey coloured peptide of psaE was detected in our previous work (Levin et al ., 2023), but not in this work. HL, high light; LL, low light.…”

“…4b). Intriguingly, the phosphorylation of Ser63 in PsaE, identified in C. ohadii cells in our earlier research (Table 1; Levin et al ., 2023), is located directly at the interface with Fd (Fig. 4c).…”

“…Chlorella ohadii attracted the photoinhibition of photosynthesis research since it is highly resistant and thrives in light conditions in which other algae and plants are bleached (Treves et al ., 2013; Levin et al ., 2023). The major mechanism of photoinhibition resistance includes a significant elimination of the outer and inner PSII antennas and the enormous accumulation of carotenoids and protective proteins (Levin et al ., 2021).…”

“…Recently, we found that when acclimated to low light (LL), Chlorella ohadii , an extremely light‐tolerant desert green alga (Treves et al ., 2016; Levin et al ., 2021; Levin & Schuster, 2023), has only limited state transitions, while when acclimated to HL, this process is absent (Levin et al ., 2023). Accordingly, PSII–LHCII protein phosphorylation in thylakoids of state II‐induced C. ohadii cells is negligible compared with other algae and plants.…”

“…Accordingly, PSII–LHCII protein phosphorylation in thylakoids of state II‐induced C. ohadii cells is negligible compared with other algae and plants. However, phosphorylation of the PSI subunit PsaE was detected in both LL Chlamydomonas reinhardtii and C. ohadii cells, but not in HL C. ohadii , suggesting possible light modulation of PSI–LHCI phosphorylation (Levin et al ., 2023). This discovery prompted an investigation of the extent, location, and possible roles of PSI–LHCI protein phosphorylation in LL‐ and HL‐grown C. ohadii cells.…”