LHCSR1-dependent fluorescence quenching is mediated by excitation energy transfer from LHCII to photosystem I in Chlamydomonas reinhardtii

Abstract

Photosynthetic organisms are frequently exposed to light intensities that surpass the photosynthetic electron transport capacity. Under these conditions, the excess absorbed energy can be transferred from excited chlorophyll in the triplet state (3Chl*) to molecular O, which leads to the production of harmful reactive oxygen species. To avoid this photooxidative stress, photosynthetic organisms must respond to excess light. In the green alga , the fastest response to high light is nonphotochemical quenching, a process that allows safe dissipation of the excess energy as heat. The two proteins, UV-inducible LHCSR1 and blue light-inducible LHCSR3, appear to be responsible for this function. While the LHCSR3 protein has been intensively studied, the role of LHCSR1 has been only partially elucidated. To investigate the molecular functions of LHCSR1 in, we performed biochemical and spectroscopic experiments and found that the protein mediates excitation energy transfer from light-harvesting complexes for Photosystem II (LHCII) to Photosystem I (PSI), rather than Photosystem II, at a low pH. This altered excitation transfer allows remarkable fluorescence quenching under high light. Our findings suggest that there is a PSI-dependent photoprotection mechanism that is facilitated by LHCSR1.

Photosystem II antenna complexes CP26 and CP29 are essential for nonphotochemical quenching in Chlamydomonas reinhardtii

“…Recent reports have pointed out that LHCSR also acts as quencher of PSI through the associated LHCII antennas (Girolomoni et al, ; Kosuge et al, ): This quenching component was also absent in k69 . Considering that both CP26 and CP29 are involved in LHCII detachment from PSII and its migration towards PSI, it is possible that LHCSR‐dependent quenching of LHCII, when detached from PSII and/or connected to PSI, may be also related to LHCSR interaction with monomeric antennas.…”

“…Additional work is required to investigate the specific role of CP26. Considering the destabilization of PSII-LHCII supercomplexes in the absence of CP26 and CP29, an alternative possibility explaining the NPQ phenotype of k9 and k69 strains is an indirect role of CP26 and CP29, which the absence might destabilize some other PSII subunits important for LHCSR1/LHCSR3 binding as quenching activity, as reported in the case of PSBR(Xue et al, 2015).Recent reports have pointed out that LHCSR also acts as quencher of PSI through the associated LHCII antennas(Girolomoni et al, 2019;Kosuge et al, 2018): This quenching component was also absent in k69. Considering that both CP26 and CP29 are involved in LHCII detachment from PSII and its migration towards PSI, it is possible that LHCSR-dependent quenching of LHCII, when detached from PSII and/or connected to PSI, may be also related to LHCSR interaction with monomeric antennas.…”

The Chlamydomonas deg1c Mutant Accumulates Proteins Involved in High Light Acclimation

“…7; Supplemental Table S1). They comprise enzymes of the CCM and photorespiration, both providing additional electron sinks (Wingler et al, 2000;Yamano et al, 2008); two ascorbate peroxidases involved in antioxidant defense (Caverzan et al, 2012); proteins with roles in photoprotection (LHCBM8; Girolomoni et al, 2017) and the transfer of excitation energy to PSI (LHCSR1; Kosuge et al, 2018); and a homolog of the Arabidopsis APE1 protein involved in acclimation to high light (Walters et al, 2003). Since most of these upregulated proteins are not localized in the stroma, they cannot be substrates of DEG1C and must be upregulated via signaling pathways responding to decreased DEG1C activity.…”

Microsecond and millisecond dynamics in the photosynthetic protein LHCSR1 observed by single-molecule correlation spectroscopy

“…Under high light (sunny), LHCs also dissipate excess energy as heat through a process known as nonphotochemical quenching (NPQ), which is activated by conformational changes (14,15). In unicellular algae and mosses, Light-Harvesting Complex Stress Related 1 (LHCSR1) is the LHC responsible for dissipation (16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27). Single-molecule spectroscopy of LHCSR1 revealed frequent transitions between bright (photoactive) and dim (quenched) states (9).…”