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Coupled iron cycling and organic matter transformation across redox interfaces

Nature Reviews Earth & Environment volume 4, pages 659–673 (2023)Cite this article

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Abstract

Soils and sediments are major reservoirs of organic matter (OM), whose dynamic turnover has a major impact on carbon cycling and global climate. OM in soils and sediments is predominantly associated with minerals, which decelerate OM decomposition and could help store carbon. However, iron (Fe) minerals could also degrade OM and release a fraction of OM to the atmosphere as CO2 and CH4, but the coupling of these processes is only partly understood. In this Review, we describe the mechanisms and importance of coupled iron–carbon (Fe–C) cycles. Oxygenation of structural Fe(II) in minerals generates reactive oxygen species, which either degrades or synthesizes OM. Reactive oxygen species can also either decrease or increase extracellular enzyme activity and microbial activity, thus indirectly transforming OM. In addition, Fe(III) reduction contributes to OM oxidation through anaerobic respiration. By contrast, OM affects the redox properties of Fe minerals by serving as electron donor, acceptor, shuttle, buffer or conductor and by co-precipitation and complexation with Fe minerals. These feedback mechanisms can result in complex interconnected Fe–C cycling processes; hence, future work must focus on attaining the net impact of combined Fe–C cycles.

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Fig. 1: Redox potentials of Fe minerals and some representative organic matter.
Fig. 2: Three example interactions among ROS, enzymes and substrate resulting in different effects on organic matter transformation.
Fig. 3: Transformation of organic matter driven by Fe redox cycling.
Fig. 4: Organic matter as an electron shuttle or electron conductor to enhance Fe(III) bioreduction.
Fig. 5: Site-specific roles of organic matter as electron donor and shuttle in expandable clay minerals.
Fig. 6: Functions of organic matter in moderating redox cycling of Fe minerals arranged into a sequence.

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (42192500 and 42192503). The authors are grateful to D. Guo for improving the quality of all figures and to D. Hu for helping with reference formatting. A.K. acknowledges infrastructural support by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy, Cluster of Excellence EXC2124, project ID 390838134.

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Authors and Affiliations

  1. Center for Geomicrobiology and Biogeochemistry Research, State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing, China

    Hailiang Dong, Qiang Zeng & Yizhi Sheng

  2. Institute of Surface-Earth System Science, School of Earth System Science, Tianjin University, Tianjin, China

    Chunmei Chen & Guanghui Yu

  3. Geomicrobiology Group, Department of Geosciences, University of Tübingen, Tübingen, Germany

    Andreas Kappler

  4. Cluster of Excellence: EXC 2124: Controlling Microbes to Fight Infection, University of Tübingen, Tübingen, Germany

    Andreas Kappler

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H.D. developed the concept and wrote the first draft. All authors contributed to editing and discussion.

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Glossary

α-Glucosidase

A carbohydrate-hydrolase that releases α-glucose.

β-Glucosidase

An enzyme that catalyses the hydrolysis reaction of cellobiose.

Autotrophic

Ability of microorganisms to produce biomass from inorganic carbon (CO2) using energy from sunlight or inorganic chemical reactions.

Fenton-like reaction

Reduction of O2 to H2O2 and subsequent reaction with Fe(II).

Heterotrophic

Ability of microorganisms to produce biomass from organic carbon.

Hydrolases

Enzymes that break down a chemical compound by reaction with water.

Microbial decomposers

A microbial community that decomposes organic matter.

Microbial necromass

Dead biomass, including all microbial products and constituting an important fraction of soil organic matter.

Mineral–OM associations

(MOAs). Mineral–organic matter association via physical and chemical interactions.

Mixotrophic

Ability of microorganisms to be either autotrophic or heterotrophic depending on the availability of carbon substrate and environmental conditions.

Oxidases

Enzymes that catalyse chemical reactions involving donation of a hydrogen atom and reduction of oxygen to form water or hydrogen peroxide.

Peroxidases

Enzymes that catalyse the oxidation of a substrate by peroxide.

Phototrophic

A special type of autotrophic lifestyle, using sunlight as a source of energy to synthesize organic compounds out of inorganic carbon (CO2).

Reactive oxygen species

(ROS). Highly reactive chemical species, owing to the presence of unpaired electrons, formed from reaction with molecular O2.

Redox potential

The thermodynamic driving force of a chemical species to be either reduced by accepting electrons or oxidized by donating electrons.

Substrate

Organic compounds that specifically bind to enzymes to support microbial growth.

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Dong, H., Zeng, Q., Sheng, Y. et al. Coupled iron cycling and organic matter transformation across redox interfaces. Nat Rev Earth Environ 4, 659–673 (2023). https://doi.org/10.1038/s43017-023-00470-5

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