Visible light induces bacteria to produce superoxide for manganese oxidation

doi:10.1007/s11783-023-1619-y

Front. Environ. Sci. Eng.

2023, Vol. 17

Issue (2) : 19 https://doi.org/10.1007/s11783-023-1619-y

RESEARCH ARTICLE

Visible light induces bacteria to produce superoxide for manganese oxidation

Fan Yang^1,², Junpeng Li^1,², Huan Wang¹, Xiaofeng Xiao^1,², Rui Bai^1,², Feng Zhao¹(

)

¹. CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China
². University of Chinese Academy of Sciences, Beijing 100049, China

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Abstract

● Term of manganese-oxidizing microorganisms should be reconsidered.

● Visible light induces heterotrophic bacteria to produce superoxide.

● Heterotrophic bacteria oxidize Mn(II) ions with a fast oxidation rate.

● Superoxide oxidizing Mn(II) ions is an unintended side reaction of bacteria.

● Superoxide is an important oxidation force of Mn(II) in the environment.

Manganese oxides are widely distributed in soils and sediments, affecting the migration and transformation of heavy metals and organic pollutants. The microbial conversion of soluble Mn(II) into insoluble Mn(III/IV) oxides is considered to be the initial source of manganese oxides in the environment; however, whether this process is related to a physiological role remains unclear. Here, we explored the microbial manganese oxidation process under visible light by using coastal surface seawater microorganisms. Visible light greatly promotes the oxidation rate of Mn(II), and the average rate reaches 64 μmol/(L·d). The generated manganese oxides were then conducive to Mn(II) oxidation, thus the rapid manganese oxidation was the result of the combined action of biotic and abiotic, and biological function accounts for 88 % ± 4 %. Extracellular superoxide produced by microorganisms induced by visible light is the decisive factor for the rapid manganese 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 unintentional 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, all these bacteria can participate in the geochemical cycle of manganese. What’s more, the superoxide oxidation pathway might be a significant natural source of manganese oxide.

Keywords Mn(II) oxidation Manganese-oxidizing bacteria Reactive oxygen species Mn(III/IV) oxides

Corresponding Author(s): Feng Zhao

About author:

Tongcan Cui and Yizhe Hou contributed equally to this work.

Issue Date: 08 September 2022

Cite this article:

Fan Yang,Junpeng Li,Huan Wang, et al. Visible light induces bacteria to produce superoxide for manganese oxidation[J]. Front. Environ. Sci. Eng., 2023, 17(2): 19.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-023-1619-y
https://academic.hep.com.cn/fese/EN/Y2023/V17/I2/19

Fig.1 Visible light promotes bacterial manganese oxidation. (a) The concentration change of Mn(III/IV) oxides with time: red and blue represent the light and dark culture conditions, respectively; solid and hollow symbols represent the bacteria and sterile control groups, respectively. Lines of dark, abiotic light, and abiotic dark groups are overlapped, due to Mn(II) oxidation has not occurred in the three groups; (b) SEM image of biogenic Mn(III/IV) oxides under light; (c) The manganese-oxidizing inhibition rate when the bacterial activity was inhibited by NaN₃ or heat treatment; (d) Change of Mn(III/IV) oxides content with time after light removal. Error bars represent the standard deviation of three replicates.

Fig.2 Community composition before and after light/dark culture with manganese (genus level). Cultures with Mn(II) ions in the dark/light are marked as dark + Mn²⁺ and light + Mn²⁺, respectively. The initial inoculum is marked as initial.

Fig.3 Changes in pH during light/dark cultures with/without manganese. Red and blue represent the light and dark culture conditions, respectively; solid and hollow symbols represent the presence and absence of Mn(II) ions, respectively. Error bars represent the standard deviation of three replicates.

Fig.4 Reactive oxygen species detection. (a) The increased fluorescence intensity ratio of light with/without Mn(II) ions and the addition of reactive oxygen species initiator (Rosup); (b) Superoxide concentrations were detected in light/dark conditions for 2 h in the presence/absence of manganese. (c) Inhibition rate of Mn(II) oxidation with different inhibitors. Error bars represent the standard deviation of three replicates.

Fig.5 Oxidation capacity of the generated Mn(III/IV) oxides. (a) Change of Mn(III/IV) oxides content with NaN₃ addition; (b) Content of Mn(III/IV) oxides before and after 6 d of light/dark culture; (c) Inhibition rate of manganese oxidation under light culture by adding the hole scavengers oxalate (1 mmol/L), sulfite (1 mmol/L). Error bars represent the standard deviation of three replicates.

Fig.6 Mechanism of manganese oxidation under light incubation.

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