Synechocystis sp. PCC 6803 Requires the Bidirectional Hydrogenase to Metabolize Glucose and Arginine Under Oxic Conditions

• Published in: Frontiers in microbiology Vol. 13; p. 896190
• Main Authors: Burgstaller, Heinrich, Wang, Yingying, Caliebe, Johanna, Hueren, Vanessa, Appel, Jens, Boehm, Marko, Leitzke, Sinje, Theune, Marius, King, Paul W., Gutekunst, Kirstin
• Format: Journal Article
• Language: English
• Published: United States Frontiers Research Foundation 31-05-2022; Frontiers Media S.A
• Subjects: arginine; BASIC BIOLOGICAL SCIENCES; diaphorase; hydrogenase; Microbiology; photomixotrophy; photosynthesis; photosynthetic complex I (NDH-1); respiration
• ISSN: 1664-302X; 1664-302X
• DOI: 10.3389/fmicb.2022.896190

The cyanobacterium
Synechocystis
sp.PCC 6803 possesses a bidirectional NiFe-hydrogenase, HoxEFUYH. It functions to produce hydrogen under dark, fermentative conditions and photoproduces hydrogen when dark-adapted cells are illuminated. Unexpectedly, we found that the deletion of the large subunit of the hydrogenase (HoxH) in
Synechocystis
leads to an inability to grow on arginine and glucose under continuous light in the presence of oxygen. This is surprising, as the hydrogenase is an oxygen-sensitive enzyme. In wild-type (WT) cells, thylakoid membranes largely disappeared, cyanophycin accumulated, and the plastoquinone (PQ) pool was highly reduced, whereas Δ
hoxH
cells entered a dormant-like state and neither consumed glucose nor arginine at comparable rates to the WT. Hydrogen production was not traceable in the WT under these conditions. We tested and could show that the hydrogenase does not work as an oxidase on arginine and glucose but has an impact on the redox states of photosynthetic complexes in the presence of oxygen. It acts as an electron valve as an immediate response to the supply of arginine and glucose but supports the input of electrons from arginine and glucose oxidation into the photosynthetic electron chain in the long run, possibly
via
the NDH-1 complex. Despite the data presented in this study, the latter scenario requires further proof. The exact role of the hydrogenase in the presence of arginine and glucose remains unresolved. In addition, a unique feature of the hydrogenase is its ability to shift electrons between NAD(H), NADP(H), ferredoxin, and flavodoxin, which was recently shown
in vitro
and might be required for fine-tuning. Taken together, our data show that
Synechocystis
depends on the hydrogenase to metabolize organic carbon and nitrogen in the presence of oxygen, which might be an explanation for its prevalence in aerobic cyanobacteria.