Origin & Evolution of Life

Early-branching Cyanobacteria Up-regulate Superoxide Dismutase Activity Under A Simulated Early Earth Anoxic Atmosphere

By Keith Cowing
Status Report
March 17, 2024
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Early-branching Cyanobacteria Up-regulate Superoxide Dismutase Activity Under A Simulated Early Earth Anoxic Atmosphere
Schematic representation of oxygenic photosynthesis and the generation of superoxide during the day inside a Cyanobacterial cell. The thylakoid membrane contains Photosystem II (PSII) connected to phycobilisomes, Photosystem I (PSI), cytochrome b6f (cyt b6f), and electron transporters plastoquinone (PQ) and plastocyanin (PC). Phycobilisomes capture light energy and transfer it to PSII resulting in the hydrolysis of water and transfer of electrons to PQ, with the concomitant generation of molecular oxygen (O2) and protons (H+ ). PQ then transfers the electrons to PSI via cyt b6f and PC, thereby translocating two protons (2H+ ) across the thylakoid membrane, into the lumen. The resulting proton gradient powers the synthesis of adenosine triphosphate (ATP) via ATP synthase. PSI transfers electrons to ferredoxin (Fd), that in turn transfers electrons to ferredoxin NADP+ oxidoreductase (FNR) to generate reduced nicotinamide adenine dinucleotide phosphate (NADPH). Both NADPH and ATP are used to power cellular processes, such as CO2 fixation (Mullineaux, 2014). Increased light exposure may result in excess electrons being fed into the electron transport chain, resulting in the generation of superoxide (O2 •– ) (Latifi et al., 2009). Dismutation of O2 •– to hydrogen peroxide (H2O2) potentially occurs in different species via superoxide dimutases (SODs), in the cytoplasm, thylakoid lumen or periplasmic space (Herbert et al., 1992; Li et al., 2002; Napoli et al., 2021; Raghavan et al., 2013; Raghavan et al., 2015). Image generated in Biorender ©. — biorxiv.org

The evolution of oxygenic photosynthesis during the Archean (4-2.5 Ga), required the presence of complementary reducing pathways to maintain the cellular redox balance.

While the timing of the evolution of superoxide dismutases (SODs), enzymes that convert superoxide to hydrogen peroxide, within the Bacteria and Archaea is not resolved, SODs containing copper and zinc in the reaction centre (CuZnSOD) were the first SODs estimated to appear in photosynthetic cyanobacteria, ≥ 2.93 Ga.

Here we analysed the SOD gene expression and activity in the deep branching strain, Pseudanabaena sp. PCC7367. It releases more O2 and exhibits significantly higher growth rates (p<0.001) and protein and glycogen contents (p<0.05) under anoxic conditions compared to control cultures grown under present oxygen rich atmospheres in low CO2 (LC) or high CO2 (HC), prompting the question as to whether this correlates to higher cellular SOD activity under anoxic Archean simulated conditions.

Expression of sodB encoding an iron containing SOD (FeSOD) and sodC, encoding a CuZnSOD, strongly correlated with increased extracellular O2 levels (p<0.001), while transcription of sodA, encoding a manganese containing (MnSOD), correlated to SOD activity during the day (p=0.019), when medium O2 concentrations were the highest.

Cytosolic SOD activity was significantly higher (p<0.001) in anoxic cultures, two hrs before nightfall compared to oxic growth conditions. Night-time combined sodABC transcription in stirred cultures was significantly reduced (p<0.05) under anoxic conditions at elevated CO2 levels, as were medium O2 levels (p≤0.001), when compared to cultures grown under present-day oxic conditions with low CO2. Total cytosolic SOD activity remained comparable, suggesting that the replacement rate of SOD is higher under modern-day conditions than on early Earth.

Our data suggest that the early branching cyanobacterium Pseudanabaena sp. PCC7367 may have retained ‘ancestral’ features permitting it to thrive in its ecological niche as a benthic mat in shallow water marine environments.

Early-branching cyanobacteria up-regulate superoxide dismutase activity under a simulated early Earth anoxic atmosphere, biorxiv.org


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