Cyanobacterial flv4-2 Operon-Encoded Proteins Optimize Light Harvesting and Charge Separation in Photosystem II

Abstract

Photosystem II (PSII) complexes drive the water-splitting reaction necessary to transform sunlight into chemical energy. However, too much light can damage and disrupt PSII. In cyanobacteria, the flv4-2 operon encodes three proteins (Flv2, Flv4, and Sll0218), which safeguard PSII activity under air-level CO2 and in high light conditions. However, the exact mechanism of action of these proteins has not been clarified yet. We demonstrate that the PSII electron transfer properties are influenced by the flv4-2 operon-encoded proteins. Accelerated secondary charge separation kinetics was observed upon expression/overexpression of the flv4-2 operon. This is likely induced by docking of the Flv2/Flv4 heterodimer in the vicinity of the QB pocket of PSII, which, in turn, increases the QB redox potential and consequently stabilizes forward electron transfer. The alternative electron transfer route constituted by Flv2/Flv4 sequesters electrons from QB(-) guaranteeing the dissipation of excess excitation energy in PSII under stressful conditions. In addition, we demonstrate that in the absence of the flv4-2 operon-encoded proteins, about 20% of the phycobilisome antenna becomes detached from the reaction centers, thus decreasing light harvesting. Phycobilisome detachment is a consequence of a decreased relative content of PSII dimers, a feature observed in the absence of the Sll0218 protein.

Cyanobacterial Oxygenic Photosynthesis is Protected by Flavodiiron Proteins

“…Compared to Synechocystis sp. PCC 6803 Flv1 and Flv3 proteins studied both in vitro and in vivo since 2002 [ 55 , 64 , 65 , 66 , 67 , 76 ] the Flv2 and Flv4 proteins have received little attention, and it has only been recently that they have been recognized as important players in PSII photoprotection [ 2 , 54 , 78 , 79 , 80 ]. The ∆ flv4 mutant cells lacking all proteins encoded by the whole operon (Flv2, Sll0218 and Flv4 proteins) demonstrate slow growth and a reduced level of PSII centers.…”

“…This route could alleviate excitation pressure by channeling excess electrons to a yet unknown electron acceptor under ambient CO 2 conditions [ 2 , 78 , 79 ]. Indeed, the Flv2/Flv4 heterodimer stabilizes forward electron transfer and increases the charge separation rate in PSII [ 80 ]. Importantly, an increased amount of singlet oxygen ( 1 O 2 ) and carotenoids in the ∆ flv4 mutant compared to the wild type, sharply contrasting the significantly decreased levels in the flv4-2 /OE overexpression strain, strongly support the idea that the Flv2/Flv4 heterodimer protects the PSII complex by decreasing 1 O 2 production [ 79 ].…”

Overexpression of plastid terminal oxidase in Synechocystis sp. PCC 6803 alters cellular redox state

“…Flv2 and Flv4 have a role comparable to that of PTOX keeping the PQ pool oxidized [27,28]. It has been recently proposed that they act also on the midpoint potential of the secondary quinone acceptor Q B thereby stabilizing forward electron transport and avoiding the generation of singlet oxygen by charge recombination reactions in PSII [29]. Furthermore, the deletion of the flv4-2 operon results in a partial detachment of the phycobilisome antenna from the PSII reaction centre ( [28,29]; for a recent review see [25]).…”

“…It has been recently proposed that they act also on the midpoint potential of the secondary quinone acceptor Q B thereby stabilizing forward electron transport and avoiding the generation of singlet oxygen by charge recombination reactions in PSII [29]. Furthermore, the deletion of the flv4-2 operon results in a partial detachment of the phycobilisome antenna from the PSII reaction centre ( [28,29]; for a recent review see [25]). In cyanobacteria that contain Flv2, Flv4 and PTOX, the physiological role of these enzymes and their interplay are unclear.…”

A novel Ca2+-binding protein influences photosynthetic electron transport inAnabaenasp. PCC 7120

“…[69]. A mutant strain lacking flv4 showed substantial phenotypic overlap with the cse-ox mutant, including increased PSII monomer:dimer ratio, over-reduction of the PQ pool and higher fluorescence emission from detached APC [69][70][71]. Furthermore, expression of flv4 in Anabaena was downregulated by a shift to low Ca 2+ conditions [30].…”