Flavodiiron proteins 1–to-4 function in versatile combinations in O2 photoreduction in cyanobacteria

Abstract

Flavodiiron proteins (FDPs) constitute a group of modular enzymes widespread in Bacteria, Archaea and Eukarya. Synechocystis sp. PCC 6803 has four FDPs (Flv1-4), which are essential for the photoprotection of photosynthesis. A direct comparison of light-induced O2 reduction (Mehler-like reaction) under high (3% CO2, HC) and low (air level CO2, LC) inorganic carbon conditions demonstrated that the Flv1/Flv3 heterodimer is solely responsible for an efficient steady-state O2 photoreduction under HC, with flv2 and flv4 expression strongly down-regulated. Conversely, under LC conditions, Flv1/Flv3 acts only as a transient electron sink, due to the competing withdrawal of electrons by the highly induced NDH-1 complex. Further, in vivo evidence is provided indicating that Flv2/Flv4 contributes to the Mehler-like reaction when naturally expressed under LC conditions, or, when artificially overexpressed under HC. The O2 photoreduction driven by Flv2/Flv4 occurs down-stream of PSI in a coordinated manner with Flv1/Flv3 and supports slow and steady-state O2 photoreduction.

Oxygen and ROS in Photosynthesis

“…In cyanobacteria [148,149], flavodiiron proteins reduce oxygen to water without ROS production. A substantial fraction of the total photosynthetic electron flow may be directed to this route [150]. Flavodiiron proteins have later been found from all oxygenic phototrophs except for angiosperms and some non-green algae (for review, see [151] (58)) if the scavenging of H 2 O 2 by the antioxidant enzymes is not fast enough for the efficient removal of H 2 O 2 .…”

Enhanced Production of D-Lactate in Cyanobacteria by Re-Routing Photosynthetic Cyclic and Pseudo-Cyclic Electron Flow

“…In Syn6803, there are 4 Flv proteins (Flv1-4), which form two distinct heterodimeric complexes (Flv1/3 and Flv2/4) with roles in oxygen reduction downstream of PSI (Zhang et al, 2012;Allahverdiyeva et al, 2013;Shimakawa et al, 2015;Santana-Sanchez et al, 2019). In addition, it remains possible that under certain conditions, all four Flv proteins might form homodimers TABLE 2 | List of all strains used or generated in this study.…”

Cytochrome cMdownscales photosynthesis under photomixotrophy inSynechocystissp. PCC 6803

“…6E). Strikingly, gross O 2 production was approximately 10 times higher compared to WT and 18 O 2 consumption in light followed a triphasic pattern, a characteristic trend reflecting the contribution of Flv1/3 and Flv2/4 to O 2 consumption in light (Santana-Sanchez et al 2019). The triphasic pattern in Δ CytM was observed as an initial burst of O 2 consumption following the dark-to-light transition, which faded after 1-1.5 min and continued at a relatively constant rate (Fig.…”

“…How Synechocystis regulates electron input from PSII and the NDH-1 and SDH complexes into the photosynthetic electron transport chain and to respiratory terminal acceptors under photomixotrophic conditions, is not fully understood. Moreover, Synechocystis encodes four isoforms of flavodiiron proteins (FDPs), Flv1-4, which likely utilize NAD(P)H (Vicente et al 2002, Brown et al 2019 or reduced Fed (Santana-Sanchez et al 2019). These proteins function in light-induced O 2 reduction as hetero-oligomers consisting of either Flv1/Flv3 or Flv2/Flv4 (Helman et al 2003, Mustila et al 2016, Allahverdiyeva et al 2015, Santana-Sanchez et al 2019.…”

“…6), O 2 and CO 2 fluxes in whole cells were monitored using MIMS (membrane inlet mass spectrometry) after enriching the samples with 18 O 2 . In contrast to a classical oxygen electrode, which determines only net O 2 changes, MIMS differentiates between gross photosynthetic O 2 production by PSII and O 2 consumption in light, mediated by flavodiiron proteins (Flv1-to-Flv4) and RTOs(Ermakova et al 2016, Santana-Sanchez et al 2019. Net O 2 production is then calculated by subtracting the rates of O 2 consumption in light from gross O 2 production.…”