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Dynamic interactions at the mineral–organic matter interface

Abstract

Minerals are widely assumed to protect organic matter (OM) from degradation in the environment, promoting the persistence of carbon in soil and sediments. In this Review, we describe the mechanisms and processes operating at the mineral–organic interface as they relate to OM transformation dynamics. A broad set of interactions occur, with minerals adsorbing organic compounds to their surfaces and/or acting as catalysts for organic reactions. Minerals can serve as redox partners for OM through direct electron transfer or by generating reactive oxygen species, which then oxidize OM. Finally, the compartmentalization of soil and sediment by minerals creates unique microsites that host diverse microbial communities. Acknowledgement of this multiplicity of interactions suggests that the general assumption that the mineral matrix provides a protective function for OM is overly simplistic. Future work must recognize adsorption as a condition for further reactions instead of as a final destination for organic adsorbates, and should consider the spatial and functional complexity that is characteristic of the environments where mineral–OM interactions are observed.

Key points

  • Minerals enable the compartmentalization of soils and sediments into small yet clearly delineated spaces, such that different chemical, ecological and evolutionary processes can occur concurrently within a larger system context.

  • Organic matter (OM) attachment to mineral surfaces is dynamic, sensitive to interfacial energies and topology, and exhibits features reminiscent of a partial wetting phenomenon.

  • Mineral-derived reactive oxygen species represent overlooked but undeniably key reactants in the oxidation and transformation of OM within soils and sediments.

  • Correlations between OM and fine-grained minerals, although generally interpreted as reflecting the impacts of minerals on OM, could additionally reflect impacts of OM on mineral nucleation, growth and transformation.

  • Depending on system logistics and environmental setting, the same type of mineral could act as a sorbent, chemical reactant and catalyst for associated OM, enabling a vast portfolio of potentially opposing outcomes.

  • Assessments regarding the fate of OM in the environment should not be derived from correlations with single predictor values, such as abundance of a certain mineral phase or specific surface area.

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Fig. 1: Organic matter cycling in soils and sediments and mineral–organic matter interactions.
Fig. 2: Organic multifunctionality.
Fig. 3: Key properties of fine-grained minerals and related solids.
Fig. 4: Size, shape and global distributions of minerals.
Fig. 5: Organic ligands at mineral interfaces.
Fig. 6: Molecular mechanisms of organic matter reactions at mineral–water interfaces.
Fig. 7: Mineral-induced organic carbon redox pathways.
Fig. 8: Compartmentalization and mineral–organic matter–microbe interactions.

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Acknowledgements

We acknowledge the constructive suggestions of the three anonymous reviewers. I.C.B. was supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, Geosciences Program under Award DE-SC0018419. S.C.B.M. was supported by the NSF (CHE; Award 1609927). C.M.H.’s contribution was supported by NSF Award EAR 1826940.

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All authors participated in developing the concept. Figures were developed by E.K.C. (Figs. 1 and 5), M.K. (Fig. 2), I.C.B. (Figs. 3 and 4), S.C.B.M. (Fig. 6), C.M.H. (Fig. 7) and N.N. (Fig. 8). All authors contributed to writing and editing.

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Correspondence to Markus Kleber.

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Glossary

Colloidal

Molecules or polymolecular particles dispersed in a medium that have at least in one direction a dimension roughly between 1 nm and 1 μm.

Poorly crystalline

An operational term to distinguish crystalline structures with short-range order from others that exhibit order over longer distances.

Unsaturated soils

(Soil) pore systems that are only partially filled with water are unsaturated; pore systems entirely filled with water are considered saturated.

Adsorption

An increase in the concentration of a dissolved substance at the interface of a condensed and a liquid or gaseous phase.

Reactive oxygen species

(ROS). Short-lived oxygen-bearing molecules with half-lives that range from fractions of seconds to days, including hydrogen peroxide (H2O2), superoxide (O2•−/HO2), hydroxyl radical (HO), singlet oxygen (1O2) and carbonate radical (CO3• −).

Compartmentalization

The division of a system into multiple subsystems with well-defined boundaries that provide a certain degree of process autonomy.

Chemotrophic

The ability to use electron donors other than photons for the synthesis of organic compounds containing reduced carbon.

Phototrophic

The ability to capture photons as an energy source for the synthesis of organic compounds containing reduced carbon.

Heterotrophic

The ability to derive nutritional requirements from complex organic substances.

Depolymerization

The disassembly of a polymer into its constituent monomers or into a mixture of products.

Fine-grained fraction

Mineral grains with an average diameter smaller than 50/63 microns, depending on the classification system used.

Coulombic interactions

Interactions that result from the electric force between two charged entities.

Dispersion

A system in which particles of colloidal size of any nature (solid, liquid or gas) are dispersed in a continuous phase of a different composition (or state).

Coagulation

The formation of aggregates from a fluid colloidal system.

Steric constraints

Factors or effects that prevent the adoption of a certain spatial orientation that would be required for the reaction to proceed unhindered.

Crystal facets

Flat planes on a crystal.

Interfacial energy

Excess free energy or work associated with the interface between two phases, per interfacial area.

Crystal growth

The addition of new atoms into the characteristic arrangement of the crystalline lattice, releasing thermal energy (enthalpy of crystallization).

Solution

A homogeneous phase that results from the mixing of two (or more) phases.

Intra-particle regions

Any parts of a particle that are not participating in surface reactions.

Xenobiotic compounds

Substances that are foreign to a given natural environment or ecosystem; usually means that organisms in the system lack adaptations for the metabolic processing of a xenobiotic compound.

Ligand

Any atom or molecule attached to a central atom, usually a metallic element, in a coordination or complex compound; if regarding part of a polyatomic molecular entity as central, then the atoms, groups or molecules bound to that part are called ligands.

Photochemical lability

The tendency of a compound to undergo a chemical reaction when exposed to light.

Nucleation

The process by which nuclei are formed in solution.

Short-range-ordered

The regular and predictable arrangement of atoms over a very short distance; in crystals, order does not persist over distances of more than a few nanometres and often extends over a distance of just a few bond lengths; short-range-ordered minerals are often also referred to as poorly crystalline minerals.

Catalyst

A substance that increases the rate of a reaction without modifying the overall standard Gibbs energy change in the reaction.

Orientational freedom

The absence of any physical restrictions to the movement and arrangement of a compound.

Steric enhancement

Factors or effects that facilitate the adoption of a certain spatial orientation that would be required for the reaction to proceed unhindered.

Mixotrophic

Deriving carbon and energy from a mix of different sources, typically, a combination of inorganic and organic compounds.

Nanowires

Proteinaceous appendages produced by microbes, particularly bacteria, that are electrically conductive.

Passivated

A surface that is unreactive owing to alteration or from the formation of a thin inert coating.

Ripening

Physical and/or structural alteration of a mineral to obtain a lower surface free energy and more energetically favourable state.

Microsites

Clearly delineated spaces within an environment with unique conditions or features in which specific microbial processes can occur.

Metabolic dependency

A form of adaptation that leads to the absence or loss of the ability to synthesize a certain metabolite essential for the organism, usually in response to an abundance of said compound in the environment.

Colloidal interactions

Interactions that are enabled when particles become so small (equivalent diameter <1–2 microns) that surface-borne electric forces between particles can effectively control their behaviour in a suspension (for instance, prevent them from settling).

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Kleber, M., Bourg, I.C., Coward, E.K. et al. Dynamic interactions at the mineral–organic matter interface. Nat Rev Earth Environ 2, 402–421 (2021). https://doi.org/10.1038/s43017-021-00162-y

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