Abstract
Oxygenic photosynthesis evolved with cyanobacteria, the ancestors of plant chloroplasts. The highly oxidizing chemistry of water splitting required concomitant evolution of efficient photoprotection mechanisms to safeguard the photosynthetic machinery. The role of flavodiiron proteins (FDPs), originally called A-type flavoproteins or Flvs, in this context has only recently been appreciated. Cyanobacterial FDPs constitute a specific protein group that evolved to protect oxygenic photosynthesis. There are four FDPs in Synechocystis sp. PCC 6803 (Flv1 to Flv4). Two of them, Flv2 and Flv4, are encoded by an operon together with a Sll0218 protein. Their expression, tightly regulated by CO2 levels, is also influenced by changes in light intensity. Here we describe the overexpression of the flv4-2 operon in Synechocystis sp. PCC 6803 and demonstrate that it results in improved photochemistry of PSII. The flv4-2/OE mutant is more resistant to photoinhibition of PSII and exhibits a more oxidized state of the plastoquinone pool and reduced production of singlet oxygen compared with control strains. Results of biophysical measurements indicate that the flv4-2 operon functions in an alternative electron transfer pathway from PSII, and thus alleviates PSII excitation pressure by channeling up to 30% of PSII-originated electrons. Furthermore, intact phycobilisomes are required for stable expression of the flv4-2 operon genes and for the Flv2/Flv4 heterodimer-mediated electron transfer mechanism. The latter operates in photoprotection in a complementary way with the orange carotenoid protein-related nonphotochemical quenching. Expression of the flv4-2 operon and exchange of the D1 forms in PSII centers upon light stress, on the contrary, are mutually exclusive photoprotection strategies among cyanobacteria.
Highlights
Oxygenic photosynthesis evolved with cyanobacteria, the ancestors of plant chloroplasts
When 1O2 of 1O2 compared production was compared between the flv4-2/OE strain and the DpsbA2 control strain, we found that overexpression of the flv4-2 operon decreased singlet oxygen production by approximately 60%
The experiments conducted with the flv4-2/OE mutants of Synechocystis clearly demonstrate that overexpression of the flv4-2 operon results in a more photoprotected phenotype in LC conditions
Summary
Oxygenic photosynthesis evolved with cyanobacteria, the ancestors of plant chloroplasts. Cyanobacteria have phycobilisomes (PBs) as light-harvesting antenna, which participate in state transitions (for review, see van Thor et al, 1998; Mullineaux and Emlyn-Jones, 2005) and nonphotochemical quenching (NPQ) of excitation energy (for review, see Bailey and Grossman, 2008) Both of these processes are involved in short-term regulation of light-harvesting processes and concomitantly function as photoprotective mechanisms. These nonphotochemical energy quenching mechanisms, have only limited capacity, and it often occurs that more electrons are excited than can be safely used in photochemistry for reduction of natural metabolic electron acceptors, under stress conditions. This particular domain composition theoretically allows NAD(P)H oxidation to be coupled with O2 reduction in the same enzyme
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