Operon flv4-flv2 Provides Cyanobacterial Photosystem II with Flexibility of Electron Transfer

Abstract

Synechocystis sp PCC 6803 has four genes encoding flavodiiron proteins (FDPs; Flv1 to Flv4). Here, we investigated the flv4-flv2 operon encoding the Flv4, Sll0218, and Flv2 proteins, which are strongly expressed under low inorganic carbon conditions (i.e., air level of CO 2 ) but become repressed at elevated CO 2 conditions. Different from FDP homodimers in anaerobic microbes, Synechocystis Flv2 and Flv4 form a heterodimer. It is located in cytoplasm but also has a high affinity to membrane in the presence of cations. Sll0218, on the contrary, resides in the thylakoid membrane in association with a high molecular mass protein complex. Sll0218 operates partially independently of Flv2/Flv4. It stabilizes the photosystem II (PSII) dimers, and according to biophysical measurements opens up a novel electron transfer pathway to the Flv2/Flv4 heterodimer from PSII. Constructed homology models suggest efficient electron transfer in heterodimeric Flv2/Flv4. It is suggested that Flv2/Flv4 binds to thylakoids in light, mediates electron transfer from PSII, and concomitantly regulates the association of phycobilisomes with PSII. The function of the flv4-flv2 operon provides many b-cyanobacteria with a so far unknown photoprotection mechanism that evolved in parallel with oxygen-evolving PSII.

Flavodiiron Protein Flv2/Flv4-Related Photoprotective Mechanism Dissipates Excitation Pressure of PSII in Cooperation with Phycobilisomes in Cyanobacteria

“…The results revealed that the absence of Flv2 and Flv4 causes slower Q A 2 oxidation compared with the wild type ( Fig. 9; Zhang et al, 2012). In line with these results, Q A 2 reoxidation was shown to be significantly faster in the flv4-2/OE mutant compared with the wild type, especially compared with DpsbA2 (Fig.…”

“…In addition, the experiments were also performed with the Dflv4 mutant, which does not express the Flv4, Sll0218, and Flv2 proteins ( Fig. 1B; Zhang et al, 2012). The latter mutant contained the kanamycin cassette in sll0217 (flv4), the first gene of the operon .…”

“…Sll0218, the 19-kD protein encoded by the flv4-2 operon, locates in the thylakoid membrane and forms a high molecular mass complex in association with unknown partners. In the model proposed by Zhang et al (2012), Sll0218 stabilizes PSII dimers and facilitates the opening of a novel electron transfer pathway through the Flv2/Flv4 heterodimer, which associates with the thylakoid membrane in light. The Flv2/Flv4 complex is also important for proper energy transfer from PBs to PSII as evidenced by a high emission peak at 685 nm in the 77K fluorescence spectra.…”

Thylakoid Terminal Oxidases Are Essential for the CyanobacteriumSynechocystissp. PCC 6803 to Survive Rapidly Changing Light Intensities

“…This was further supported by investigations in Synechococcus, in which deletion of COX and COX/ARTO resulted in 1.7-and 2.2-fold increases, respectively, in the reduction rate of PSI (Nomura et al, 2006). Alternative electron sinks, such as the Flv2/Flv4 complex, which accepts electrons directly from PSII (Zhang et al, 2012), the hydrogenase complex, nitrate reductase, or carbon fixation, may compensate for the loss of terminal oxidase activity, as demonstrated by increased hydrogen production in a Synechocystis COX/Cyd-deficient strain (Gutthann et al, 2007). Energization of both the thylakoid and cytoplasmic membrane electron transfer chains is important under conditions of salt stress in Synechocystis (Jeanjean et al, 1990(Jeanjean et al, , 1993Peschek et al, 1994) and Synechococcus sp.…”

Regulation of the photosynthetic apparatus under fluctuating growth light

“…Another important difference in the photoprotection strategies of higher plants and cyanobacteria is a unique valve in the latter, composed of the Flv2/Flv4 heterodimer and the Sll0218 protein, which provides extra capacity for directing electrons away from PSII. The valve subunits accumulate under conditions that induce excess reduction of the ETC [46] that pose a potential hazard to the ETC and in particular to PSI.…”