Photoprotective auxiliary electron transport pathways in cyanobacteria

Abstract

Cyanobacteria perform oxygenic photosynthesis to fulfill their energy needs in highly dynamic environmental conditions. This requires tight regulation of photosynthetic light reactions for maintenance and optimization of the photosynthetic performance. In this thesis work, I focus on the auxiliary components assisting in the regulation and protection of photosynthetic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Even though light is essential for photosynthesis, excess excitation energy may lead to the formation of reactive oxygen species (ROS) in reaction centers, electron transfer chain and light harvesting antenna systems. In order to prevent the formation of ROS and subsequent damage to the photosynthetic apparatus, cyanobacteria rely on a number of different photoprotective mechanisms. They control the amount of excitation energy reaching the photosynthetic reaction centers and have a capacity to direct excited electrons to several alternative electron transfer routes, many of which utilize O2 as the terminal electron acceptor. Especially under conditions where the production of photosynthetic electrons exceeds their metabolic need, cyanobacteria use so-called electron valves to safely dissipate the excess electrons.

The flavodiiron proteins Flv1 and Flv3 have a capacity to function as a major alternative photosynthetic electron sink and perform O2 photoreduction without accumulating ROS. In this work, I show that Flv1 and Flv3 are indispensable during sudden changes in light intensity, as they prevent the over-reduction of the linear electron transport. The Flv1 and Flv3 proteins safeguard photosystem I, and are thus crucial for the survival of cyanobacteria under fluctuating light, a typical light condition in aquatic environments. Both the Flv1 and Flv3 proteins are essential for O2 photoreduction, and they are probably organized as a hetero-oligomer in order to function. Additionally, homo-oligomers of Flv3 are involved in the acclimation of cells to fluctuating light, and mediate a yet unidentified electron transfer pathway.

The two other flavodiiron proteins in Synechocystis, which form a Flv2/Flv4 heterodimer, have been shown to play a role as an electron sink on the acceptor side of photosystem II. These proteins are encoded by the flv4-2 operon, together with Sll0218, a small membrane protein. I demonstrate that the flv4-2 operon is transcriptionally controlled by the transcriptionl factor NdhR, and post-transcriptionally by several antisense RNAs. The accumulation of the flv4-2 operon mRNA and one of the antisense RNAs, As1_flv4, was found to be inversely correlated. The As1_flv4 prevents the premature expression of the flv4-2 operon-encoded proteins, and the Flv2/4 electron valve is synthetized only if inorganic carbon limitation continues.

Cyanobacteria have several ferredoxins that play a role in photosynthetic electron transfer and environmental stress tolerance. In this thesis work, I show that a bacterial-type ferredoxin 7 (Fed7) is important for the redox regulation of Synechocystis. Cells lacking Fed7 cannot properly respond to combined inorganic carbon limitation and high light stress. It is possible that Fed7 mediates the redox signals from the photosynthetic linear electron transport chain and functions indirectly as a redox-dependent regulator.