Study: Visible light induces bacteria to produce manganese-oxidizing superoxide

Manganese oxides are naturally reactive metals and are widespread in aquatic and terrestrial environments, affecting the fate of minerals (such as As³⁺ and Cd²⁺) and organic pollutants (such as phenols and diclofenac) through adsorption and oxidation in wastewater treatment. Usually, manganese (III/IV) oxides in the environment are thought to be formed by oxidation of dissolved manganese (II) through abiotic or biotic processes.

The oxidation of hydrated manganese(II) with dissolved oxygen is thermodynamically favored, but the kinetics are slow due to the high energy barrier of the reaction from dissolved Mn(II) to Mn(III/IV) oxides. The presence of microorganisms accelerates the oxidation rate, which is 4-5 orders of magnitude faster than the rate of abiotic chemical oxidation, so it is considered the primary source of manganese oxides in the environment.

Bacteria capable of catalyzing the oxidation of dissolved Mn(II) ions to insoluble Mn(III/IV) oxides are usually called manganese-oxidizing bacteria. Bacterial oxidation of Mn (II) ions is divided into direct and indirect methods, and the process catalyzed by enzymes on the surface of microorganisms is called direct oxidation. For indirect pathways, some bacteria can alter the environmental conditions around them in order to oxidize Mn(II) (for example, pH and Eh).

Clyde Roseobacter has been shown to oxidize manganese(II) by producing extracellular reactive oxygen species in recent studies. Do other bacteria have similar Mn(II) oxidation processes with Roseobacter? Is Mn(II) oxidation relevant to the physiological process of bacteria?

To answer these questions, Professor Feng Zhao of the Chinese Academy of Sciences and his team members explored the process of microbial manganese oxidation under visible light using coastal seawater microorganisms. The relationship between the transformation of soluble manganese (II) into insoluble manganese oxides (III/IV) by microorganisms and the physiological role was analyzed. This study has been published in Frontiers of environmental science and engineering in 2023.

In this study, the research team found that visible light significantly enhances the rate of manganese (II) oxidation, with the average rate reaching 64 μmol/(l d). The generated Mn oxides were then lead to Mn(II) oxidation, thus the rapid Mn oxidation was the result of the combined work of the biotic, abiotic and biological function calculations of 88% ± 4%.

The extracellular superoxide produced by microorganisms induced by visible light is the critical factor for rapid Mn oxidation in our study. But the production of these superoxides does not require the presence of Mn (II) ions, the Mn (II) oxidation process was more like an unintended side reaction, which did not affect the growth of microorganisms.

More than 70% of heterotrophic microorganisms in nature are capable of producing superoxide, based on the oxidizing properties of free radicals, and all of these bacteria can participate in the manganese geochemical cycle. Moreover, the superoxide pathway may be an important natural source of manganese oxide.

This study revealed an essential pathway for bacterial manganese oxidation. Heterotrophic bacteria produce superoxide under visible light irradiation and oxidize Mn(II) ions in the surrounding environment, which are the main source of manganese oxides. The biogenerated Mn(III/IV) oxides can indirectly oxidize Mn(II) ions through abiotic reactions under light illumination.

Many bacteria in the environment that actively or passively produce superoxides may also oxidize Mn(II) in this way, indicating that the Mn oxidation pathway via superoxide is a common behavior in the environment. In light of the redox properties and semiconducting properties of manganese oxides, this research will provide new ideas to address environmental pollution.