Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light

Abstract

Cyanobacterial flavodiiron proteins (FDPs; A-type flavoprotein, Flv) comprise, besides the β-lactamase–like and flavodoxin domains typical for all FDPs, an extra NAD(P)H:flavin oxidoreductase module and thus differ from FDPs in other Bacteria and Archaea. Synechocystis sp. PCC 6803 has four genes encoding the FDPs. Flv1 and Flv3 function as an NAD(P)H:oxygen oxidoreductase, donating electrons directly to O 2 without production of reactive oxygen species. Here we show that the Flv1 and Flv3 proteins are crucial for cyanobacteria under fluctuating light, a typical light condition in aquatic environments. Under constant-light conditions, regardless of light intensity, the Flv1 and Flv3 proteins are dispensable. In contrast, under fluctuating light conditions, the growth and photosynthesis of the Δ flv1(A) and/or Δ flv3(A) mutants of Synechocystis sp. PCC 6803 and Anabaena sp. PCC 7120 become arrested, resulting in cell death in the most severe cases. This reaction is mainly caused by malfunction of photosystem I and oxidative damage induced by reactive oxygen species generated during abrupt short-term increases in light intensity. Unlike higher plants that lack the FDPs and use the Proton Gradient Regulation 5 to safeguard photosystem I, the cyanobacterial homolog of Proton Gradient Regulation 5 is shown not to be crucial for growth under fluctuating light. Instead, the unique Flv1/Flv3 heterodimer maintains the redox balance of the electron transfer chain in cyanobacteria and provides protection for photosystem I under fluctuating growth light. Evolution of unique cyanobacterial FDPs is discussed as a prerequisite for the development of oxygenic photosynthesis.

Flavodiiron Proteins Promote Fast and Transient O2 Photoreduction in Chlamydomonas

“…This might be due to a differential effect on intron splicing depending on the location of the insertion in the intron. Similar patterns of accumulation were previously observed for the Flv1 protein in the Synechocystis flv3 mutant (Allahverdiyeva et al, 2013) and for the FlvA protein in the P. patens flvb mutant (Gerotto et al, 2016), which were interpreted by the existence of a functional heterodimer between Flv1 and Flv3 in Synechocystis and between FlvA and FlvB in P. patens.…”

“…The physiological function of the different O 2 photoreduction pathways has been controversial, since they have been alternatively viewed as futile pathways resulting in a waste of energy, as protective mechanisms avoiding photooxidative damage, or as a mean to (re)-equilibrate the balance between reducing and phosphorylating powers through pseudocyclic photophosphorylations (Badger, 1985;Allen, 2003). In cyanobacteria, flavodiiron proteins catalyze NADPH-dependent reduction of O 2 at the PSI acceptor side (Vicente et al, 2002;Helman et al, 2003;Allahverdiyeva et al, 2013). The Synechocystis sp.…”

“…In cyanobacteria, the PGR5/PGRL1-dependent CEF is not functional, and it was proposed that growth under fluctuating light relies on the presence of Flv1 and Flv3 that would act as an electron sink preventing overreduction of PSI acceptors and production of reactive oxygen species (Allahverdiyeva et al, 2013). Algae and mosses harbor both Flvs and PGRL1/ PGR5 CEF components (Tolleter et al, 2011;Dang et al, 2014;Johnson et al, 2014;Gerotto et al, 2016).…”

Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation

“…By consequence, no intermediary ROS compounds are formed in cyanobacteria (Allahverdiyeva et al 2013(Allahverdiyeva et al , 2015. With no ROS compounds formed, the hypothesis was put up that for cyanobacteria the need to handle the ROS compounds superoxide and HP is less compulsory than in green algae, and hence that cyanobacteria are likely more sensitive to HP than eukaryotic algae.…”

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

“…Flavodiiron proteins (FDPs), originally called A-type flavoproteins or Flvs (Wasserfallen et al, 1998), were recently demonstrated to have an important role in photoprotection of the photosynthetic machinery (Zhang et al, 2009Allahverdiyeva et al, 2011Allahverdiyeva et al, , 2013Ermakova et al, 2013). FDPs in general are most widespread among strict and facultative anaerobic bacteria.…”