de Beer, D. | bioRxiv Science

bioRxiv2024

The interplay between light, arsenic and H2O2 controls oxygenic photosynthesis in a Precambrian analog cyanobacterial mat.

The delayed rise of atmospheric oxygen, despite the early evolution of oxygenic photosynthesis (OP), remains a central puzzle in Earth history. Numerous ecological and geochemical constraints on OP have been proposed, but the role of environmental stressors at the physiological and ecosystem level is poorly understood. Here we show that Chl-f-harboring cyanobacteria in a high-altitude Andean microbial mat - an analog for Precambrian ecosystems - switch from OP to arsenite-driven anoxygenic photosynthesis (AP) under high light. Using microsensor profiling, mat incubations, and metatranscriptomics, we show that this shift is triggered by the accumulation of reactive oxygen species (ROS), especially hydrogen peroxide, which suppresses OP. Instead of ceasing activity, cyanobacteria reroute electron flow, using arsenite as the electron donor to sustain photosynthesis while avoiding both intracellular ROS from OP and extracellular ROS from aerobic arsenite oxidation. This switch is reversible and coordinated with diel cycles of light and arsenic speciation, sustained by a cryptic arsenic redox cycle, continuously regenerating arsenite for AP. Although the enzymatic basis remains unresolved, these findings reveal a hidden layer of metabolic plasticity in cyanobacteria and suggest that oxidative stress-responsive metabolic shifts may have supported early phototroph survival while limiting oxygen release - potentially contributing to Earths protracted oxygenation.

biochemistry↗

bioRxiv2018

Photosynthesis under very high oxygen concentrations in dense microbial mats and biofilms

Using microsensors O2 concentrations were measured in photosynthetically active microbial mats of up to 3 mM, corresponding to a partial pressure of 3 bar. This could damage mats by internal gas formation, and be inhibitory by formation of reactive oxygen species (ROS) and reduced effectivity of RuBisCo. The reliability of the electrochemical microsensors was checked by creating elevated O2 concentrations in a water volume placed inside a pressure tank. A microsensor mounted with the tip in the gassed water bath showed a response linearly proportional to 5.5 mM corresponding to 4 bar pure O2 pressure. After release of the pressure the O2 concentration reduced quickly to 2.5 mM, then stabilized and subsequently reduced slowly over 14 hours to approximately 2 mM. We concluded that the very high O2 concentrations measured in phototrophic microbial mats are real and O2 oversaturation in mats is a stable phenomenon. As consequence of high O2 concentrations, net production of H2O2 occurred. The accumulation was, however, limited to the respiratory zone under the photosynthetic layer. Despite the high gas pressure inside mats, no disruption of the mat structure was apparent by bubble formation inside the mats,and bubbles were only observed at mat surfaces. Additions of H2O2 to high concentrations in the water column were efficiently removed in the photosynthetically active zone. As the removal rate was linearly proportional to the H2O2 influx, this removal occurred possibly not enzymatically but by abiotic processes. Phototrophic microorganisms can produce O2 at high rates under strongly elevated O2 levels, despite the decreased efficiency due to the unfavorable kinetics of RuBisCo and energy costs for protection. Under non-limiting light conditions, this apparent dilemma is, however, not disadvantageous.\n\nImportanceBiofilms are often used in photobioreactors for production of biomass, food or specialty chemistry. Photosynthesis rates can be limited by high O2 levels or high O2/CO2 ratios which are especially enhanced in biofilms and mats, due to mass transfer limitations. High O2 may lead to reactive O2 species (ROS) and reduce the efficiency of RuBisCo. Moreover, gas formation may destabilize their structure. Here we show that extremely high levels of O2 are possible in mats and biofilms without ebullition, and while maintaining very high photosynthetic activity.

microbiology↗