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Light-independent anaerobic microbial oxidation of manganese driven by an electrosyntrophic coculture

Abstract

Anaerobic microbial manganese oxidation (AMMO) has been considered an ancient biological metabolism for Mn element cycling on Archaean Earth before the presence of oxygen. A light-dependent AMMO was recently observed under strictly anoxic conditions, providing a new proxy for the interpretation of the evolution of oxygenic photosynthesis. However, the feasibility of biotic Mn(II) oxidation in dark geological habitats that must have been abundant remains unknown. Therefore, we discovered that it would be possible to achieve AMMO in a light-independent electrosyntrophic coculture between Rhodopseudomonas palustris and Geobacter metallireducens. Transmission electron microscopy analysis revealed insoluble particle formation in the coculture with Mn(II) addition. X-ray diffraction and X-ray photoelectron spectroscopy analysis verified that these particles were a mixture of MnO2 and Mn3O4. The absence of Mn oxides in either of the monocultures indicated that the Mn(II)-oxidizing activity was induced via electrosyntrophic interactions. Radical quenching and isotopic experiments demonstrated that hydroxyl radicals (•OH) produced from H2O dissociation by R. palustris in the coculture contributed to Mn(II) oxidation. All these findings suggest a new, symbiosis-dependent and light-independent AMMO route, with potential importance to the evolution of oxygenic photosynthesis and the biogeochemical cycling of manganese on Archaean and modern Earth.

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Fig. 1: Manganese oxide formation in electrosyntrophic cocultures of G. metallireducens and R. palustris.
Fig. 2: Characteristics of insoluble manganese oxides.
Fig. 3: ROS generation in G. metallireducens and R. palustris cocultures.
Fig. 4: •OH identification and mass spectra of DMPO/•OH in G. metallireducens and R. palustris cocultures.
Fig. 5: Strategy of light-independent AMMO in G. metallireducens and R. palustris cocultures under dark and anoxic conditions.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China, Grant no. 42177270 and 42077218, the China Postdoctoral Science Foundation, grant no. 2021M700879, Guangdong Basic and Applied Basic Research Foundation, Grant no. 2021A1515110918.

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LH, XL, YY, and SZ conceived and designed the study; LH performed the experiments, collected the data, and drew all figures. YY and XL wrote the manuscript; XL, YY, CR, SZ, and KN analyzed and interpreted the data; CR and KN revised the manuscript. All authors reviewed, revised, and approved the final manuscript.

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Correspondence to Yong Yuan.

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Huang, L., Liu, X., Rensing, C. et al. Light-independent anaerobic microbial oxidation of manganese driven by an electrosyntrophic coculture. ISME J 17, 163–171 (2023). https://doi.org/10.1038/s41396-022-01335-3

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