Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Dynamic interactions at the mineral–organic matter interface


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. 1.

    Friedlingstein, P. et al. Global carbon budget 2019. Earth Syst. Sci. Data 11, 1783–1838 (2019).

    Google Scholar 

  2. 2.

    Henin, S. & Turc, L. Studies in the fractionation of soil organic matter. (1). Trans. 4th Int. Cong. Soil Sci. 1, 152–154 (1950).

    Google Scholar 

  3. 3.

    Kleber, M. et al. in Advances in Agronomy Vol. 130 (ed. Sparks, D. L.) 1–140 (Elsevier, 2015).

  4. 4.

    Jacks, G. V. The biological nature of soil productivity. Soils Fertil. 26, 147–150 (1963).

    Google Scholar 

  5. 5.

    Carson, R. Silent Spring (Houghton Mifflin, 1962).

  6. 6.

    Stone, A. T. & Morgan, J. J. Reduction and dissolution of manganese (III) and manganese (IV) oxides by organics. 1. Reaction with hydroquinone. Environ. Sci. Technol. 18, 450–456 (1984).

    Google Scholar 

  7. 7.

    Stone, A. T. & Morgan, J. J. Reduction and dissolution of manganese (III) and manganese (IV) oxides by organics. 2. Survey of the reactivity of organics. Environ. Sci. Technol. 18, 617–624 (1984).

    Google Scholar 

  8. 8.

    McBride, M. B. Reactivity of adsorbed and structural iron in hectorite as indicated by oxidation of benzidine. Clays Clay Miner. 27, 224–230 (1979).

    Google Scholar 

  9. 9.

    Parton, W. J., Schimel, D. S., Cole, C. V. & Ojima, D. S. Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Sci. Soc. Am. J. 51, 1173–1179 (1987).

    Google Scholar 

  10. 10.

    Oades, J. M. The retention of organic matter in soils. Biogeochemistry 5, 35–70 (1988).

    Google Scholar 

  11. 11.

    Jardine, P. M., Weber, N. L. & McCarthy, J. F. Mechanisms of dissolved organic carbon adsorption on soil. Soil Sci. Soc. Am. J. 53, 1378–1385 (1989).

    Google Scholar 

  12. 12.

    Gu, B., Schmitt, J., Chen, Z., Liang, L. & McCarthy, J. F. Adsorption and desorption of natural organic matter on iron oxide: mechanisms and models. Environ. Sci. Technol. 28, 38–46 (1994).

    Google Scholar 

  13. 13.

    Hedges, J. I. The formation and clay mineral reactions of melanoidins. Geochim. Cosmochim. Acta 42, 69–76 (1978).

    Google Scholar 

  14. 14.

    Rasmussen, C. et al. Beyond clay: towards an improved set of variables for predicting soil organic matter content. Biogeochemistry 137, 297–306 (2018).

    Google Scholar 

  15. 15.

    Torn, M. S., Trumbore, S. E., Chadwick, O. A., Vitousek, P. M. & Hendricks, D. M. Mineral control of soil organic carbon storage and turnover. Nature 389, 170–173 (1997).

    Google Scholar 

  16. 16.

    Chenu, C. & Plante, A. F. Clay-sized organo-mineral complexes in a cultivation chronosequence: revisiting the concept of the ‘primary organo-mineral complex’. Eur. J. Soil Sci. 57, 596–607 (2006).

    Google Scholar 

  17. 17.

    Baveye, P. C. et al. Emergent properties of microbial activity in heterogeneous soil microenvironments: different research approaches are slowly converging, yet major challenges remain. Front. Microbiol. 9, 1929 (2018).

    Google Scholar 

  18. 18.

    Oades, J. M. in Minerals in Soil Environments Vol. 1 2nd edn (eds Dixon, J. B. & Weed, S. B.) 89–160 (Soil Science Society of America, 1989).

  19. 19.

    Batjes, N. H. Total carbon and nitrogen in the soils of the world. Eur. J. Soil Sci. 47, 151–163 (1996).

    Google Scholar 

  20. 20.

    Jobbagy, E. G. & Jackson, R. B. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol. Appl. 10, 423–436 (2000).

    Google Scholar 

  21. 21.

    Vereecken, H., Maes, J., Feyen, J. & Darius, P. Estimating the soil-moisture retention characteristic from texture, bulk-density, and carbon content. Soil Sci. 148, 389–403 (1989).

    Google Scholar 

  22. 22.

    Sposito, G. The Chemistry of Soils 3rd edn (Oxford Univ. Press, 2016).

  23. 23.

    Ball, P. Water is an active matrix of life for cell and molecular biology. Proc. Natl Acad. Sci. USA 114, 13327–13335 (2017).

    Google Scholar 

  24. 24.

    Schimel, J. et al. in 19th World Congress of Soil Science, Soil Solutions for a Changing World 55–58 (International Union of Soil Sciences, 2010).

  25. 25.

    Meysman, F. J. R., Middelburg, J. J. & Heip, C. H. R. Bioturbation: a fresh look at Darwin’s last idea. Trends Ecol. Evol. 21, 688–695 (2006).

    Google Scholar 

  26. 26.

    Miller, S. L. A production of amino acids under possible primitive earth conditions. Science 117, 528–529 (1953).

    Google Scholar 

  27. 27.

    Heck, P. R. et al. The fall, recovery, classification, and initial characterization of the Hamburg, Michigan H4 chondrite. Meteorit. Planet Sci. 55, 2341–2359 (2020).

    Google Scholar 

  28. 28.

    Lengeler, J. W., Drews, G. & Schlegel, H. G. Biology of the Prokaryotes Vol. 984 (Wiley-Blackwell, 1999).

  29. 29.

    Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    Google Scholar 

  30. 30.

    Hedges, J. I. & Oades, J. M. Comparative organic geochemistries of soils and marine sediments. Org. Geochem. 27, 319–361 (1997).

    Google Scholar 

  31. 31.

    Anslyn, E. V. & Dougherty, D. A. Modern Physical Organic Chemistry (University Science Books, 2006).

  32. 32.

    Fagel, N. in Developments in Marine Geology Ch. 4 139–184 (Elsevier, 2007).

  33. 33.

    Ito, A. & Wagai, R. Global distribution of clay-size minerals on land surface for biogeochemical and climatological studies. Sci. Data 4, 170103 (2017).

    Google Scholar 

  34. 34.

    Barron, V. & Torrent in EMU Notes in Mineralogy Vol. 14 297–336 (2013).

  35. 35.

    Schulthess, C. P. & Sparks, D. L. A critical assessment of surface adsorption models. Soil Sci. Soc. Am. J. 52, 92–97 (1988).

    Google Scholar 

  36. 36.

    Heil, D. & Sposito, G. Organic matter role in illitic soil colloids flocculation: II. Surface charge. Soil Sci. Soc. Am. J. 57, 1246–1253 (1993).

    Google Scholar 

  37. 37.

    Quirk, J. P. in Advances in Agronomy Vol. 53 (ed. Sparks, D. L.) 121–183 (Elsevier, 1994).

  38. 38.

    Brown, G. E. et al. Metal oxide surfaces and their interactions with aqueous solutions and microbial organisms. Chem. Rev. 99, 77–174 (1999).

    Google Scholar 

  39. 39.

    Armanious, A., Aeppli, M. & Sander, M. Dissolved organic matter adsorption to model surfaces: adlayer formation, properties, and dynamics at the nanoscale. Environ. Sci. Technol. 48, 9420–9429 (2014).

    Google Scholar 

  40. 40.

    Petridis, L. et al. Spatial arrangement of organic compounds on a model mineral surface: implications for soil organic matter stabilization. Environ. Sci. Technol. 48, 79–84 (2014).

    Google Scholar 

  41. 41.

    Sanderman, J., Maddern, T. & Baldock, J. Similar composition but differential stability of mineral retained organic matter across four classes of clay minerals. Biogeochemistry 121, 409–424 (2014).

    Google Scholar 

  42. 42.

    Mueller, C. W. et al. Microscale soil structures foster organic matter stabilization in permafrost soils. Geoderma 293, 44–53 (2017).

    Google Scholar 

  43. 43.

    Deen, W. M. Hindered transport of large molecules in liquid-filled pores. AIChE J. 33, 1409–1425 (1987).

    Google Scholar 

  44. 44.

    McBride, M. B. Mobility of small molecules in interlayers of hectorite gels: ESR study with an uncharged spin probe. Clays Clay Miner. 42, 455–461 (1994).

    Google Scholar 

  45. 45.

    Pignatello, J. J. & Xing, B. S. Mechanisms of slow sorption of organic chemicals to natural particles. Environ. Sci. Technol. 30, 1–11 (1996).

    Google Scholar 

  46. 46.

    Yang, J. Q., Zhang, X., Bourg, I. C. & Stone, H. A. 4D imaging reveals mechanisms of clay-carbon protection and release. Nat. Commun. 12, 622 (2021).

    Google Scholar 

  47. 47.

    Navrotsky, A. Energetic clues to pathways to biomineralization: precursors, clusters, and nanoparticles. Proc. Natl Acad. Sci. USA 101, 12096–12101 (2004).

    Google Scholar 

  48. 48.

    Waychunas, G. A., Kim, C. S. & Banfield, J. F. Nanoparticulate iron oxide minerals in soils and sediments: unique properties and contaminant scavenging mechanisms. J. Nanopart. Res. 7, 409–433 (2005).

    Google Scholar 

  49. 49.

    Zucker, R. V., Chatain, D., Dahmen, U., Hagege, S. & Carter, W. C. New software tools for the calculation and display of isolated and attached interfacial-energy minimizing particle shapes. J. Mater. Sci. 47, 8290–8302 (2012).

    Google Scholar 

  50. 50.

    Sposito, G. The Surface Chemistry of Natural Particles (Oxford Univ. Press, 2004).

  51. 51.

    Pauling, L. The structure of micas and related materials. Proc. Natl Acad. Sci. USA 16, 123–129 (1930).

    Google Scholar 

  52. 52.

    Chen, J. J. et al. Building two-dimensional materials one row at a time: Avoiding the nucleation barrier. Science 362, 1135–1139 (2018).

    Google Scholar 

  53. 53.

    Venema, P., Hiemstra, T., Weidler, P. G. & Van Riemsdijk, W. H. Intrinsic proton affinity of reactive surface groups of metal (hydr)oxides: application to iron (hydr)oxides. J. Colloid Interface Sci. 198, 282–295 (1998).

    Google Scholar 

  54. 54.

    Sollins, P., Homann, P. & Caldwell, B. A. Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74, 65–105 (1996).

    Google Scholar 

  55. 55.

    Abramoff, R. et al. The Millennial model: in search of measurable pools and transformations for modeling soil carbon in the new century. Biogeochemistry 137, 51–71 (2018).

    Google Scholar 

  56. 56.

    Blankinship, J. C., Becerra, C. A., Schaeffer, S. M. & Schimel, J. P. Separating cellular metabolism from exoenzyme activity in soil organic matter decomposition. Soil Biol. Biochem. 71, 68–75 (2014).

    Google Scholar 

  57. 57.

    Chen, C., Hall, S. J., Coward, E. & Thompson, A. Iron-mediated organic matter decomposition in humid soils can counteract protection. Nat. Commun. 11, 2255 (2020).

    Google Scholar 

  58. 58.

    Leinemann, T. et al. Multiple exchange processes on mineral surfaces control the transport of dissolved organic matter through soil profiles. Soil Biol. Biochem. 118, 79–90 (2018).

    Google Scholar 

  59. 59.

    Newcomb, C. J., Qafoku, N. P., Grate, J. W., Bailey, V. L. & De Yoreo, J. J. Developing a molecular picture of soil organic matter–mineral interactions by quantifying organo–mineral binding. Nat. Commun. 8, 396 (2017).

    Google Scholar 

  60. 60.

    Ding, Y. et al. Chemodiversity of soil dissolved organic matter. Environ. Sci. Technol. 54, 6174–6184 (2020).

    Google Scholar 

  61. 61.

    Kellerman, A. M. et al. Unifying concepts linking dissolved organic matter composition to persistence in aquatic ecosystems. Environ. Sci. Technol. 52, 2538–2548 (2018).

    Google Scholar 

  62. 62.

    Teppen, B. J. & Aggarwal, V. Thermodynamics of organic cation exchange selectivity in smectites. Clays Clay Miner. 55, 119–130 (2007).

    Google Scholar 

  63. 63.

    MacKay, A. A. & Vasudevan, D. Polyfunctional ionogenic compound sorption: challenges and new approaches to advance predictive models. Environ. Sci. Technol. 46, 9209–9223 (2012).

    Google Scholar 

  64. 64.

    Ni, J. & Pignatello, J. J. Charge-assisted hydrogen bonding as a cohesive force in soil organic matter: water solubility enhancement by addition of simple carboxylic acids. Environ. Sci. Process. Impacts 20, 1225–1233 (2018).

    Google Scholar 

  65. 65.

    Schwartzenbach, R. P., Gschwend, P. M. & Imboden, D. M. Environmental Organic Chemistry (Wiley, 2016).

  66. 66.

    Sposito, G. et al. Surface geochemistry of the clay minerals. Proc. Natl Acad. Sci. USA 96, 3358–3364 (1999).

    Google Scholar 

  67. 67.

    Willemsen, J. A. R., Myneni, S. C. B. & Bourg, I. C. Molecular dynamics simulations of the adsorption of phthalate esters on smectite clay surfaces. J. Phys. Chem. C 123, 13624–13636 (2019).

    Google Scholar 

  68. 68.

    Wershaw, R. L. Model for humus in soils and sediments. Environ. Sci. Technol. 27, 814–816 (1993).

    Google Scholar 

  69. 69.

    Kleber, M., Sollins, P. & Sutton, R. A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry 85, 9–24 (2007).

    Google Scholar 

  70. 70.

    Huang, X. Z. et al. Direct evidence for thickening nanoscale organic films at soil biogeochemical interfaces and its relevance to organic matter preservation. Environ. Sci. Nano 7, 2747–2758 (2020).

    Google Scholar 

  71. 71.

    Ohno, T. & Kubicki, J. D. Adsorption of organic acids and phosphate to an iron (oxyhydr)oxide mineral: a combined experimental and density functional theory study. J. Phys. Chem. A 124, 3249–3260 (2020).

    Google Scholar 

  72. 72.

    Bowden, J. W., Posner, A. M. & Quirk, J. P. Ionic adsorption on variable charge mineral surfaces. Theoretical charge development and titration curves. Soil Res. 15, 121–136 (1977).

    Google Scholar 

  73. 73.

    Riedel, T., Biester, H. & Dittmar, T. Molecular fractionation of dissolved organic matter with metal salts. Environ. Sci. Technol. 46, 4419–4426 (2012).

    Google Scholar 

  74. 74.

    Possinger, A. R. et al. Organo–organic and organo–mineral interfaces in soil at the nanometer scale. Nat. Commun. 11, 6103 (2020).

    Google Scholar 

  75. 75.

    Mitchell, P. J., Simpson, A. J., Soong, R. & Simpson, M. J. Nuclear magnetic resonance analysis of changes in dissolved organic matter composition with successive layering on clay mineral surfaces. Soil Syst. 2, 8 (2018).

    Google Scholar 

  76. 76.

    Coward, E. K., Ohno, T. & Sparks, D. L. Direct evidence for temporal molecular fractionation of dissolved organic matter at the iron oxyhydroxide interface. Environ. Sci. Technol. 53, 642–650 (2019).

    Google Scholar 

  77. 77.

    Hatton, P.-J., Remusat, L., Zeller, B., Brewer, E. A. & Derrien, D. NanoSIMS investigation of glycine-derived C and N retention with soil organo-mineral associations. Biogeochemistry 125, 303–313 (2015).

    Google Scholar 

  78. 78.

    Lehmann, J. et al. Spatial complexity of soil organic matter forms at nanometre scales. Nat. Geosci. 1, 238–242 (2008).

    Google Scholar 

  79. 79.

    Vogel, C. et al. Submicron structures provide preferential spots for carbon and nitrogen sequestration in soils. Nat. Commun. 5, 2947 (2014).

    Google Scholar 

  80. 80.

    Shaker, A. M., Komy, Z. R., Heggy, S. E. & El-Sayed, M. E. Kinetic study for adsorption humic acid on soil minerals. J. Phys. Chem. A 116, 10889–10896 (2012).

    Google Scholar 

  81. 81.

    Koopal, L., Tan, W. F. & Avena, M. Mixed ad/desorption kinetics unraveled with the equilibrium adsorption isotherm. Colloids Surf. A Physicochem. Eng. Asp. 577, 709–722 (2019).

    Google Scholar 

  82. 82.

    Avena, M. J. & Wilkinson, K. J. Disaggregation kinetics of a peat humic acid: mechanism and pH effects. Environ. Sci. Technol. 36, 5100–5105 (2002).

    Google Scholar 

  83. 83.

    Li, W. L. et al. Real-time evaluation of natural organic matter deposition processes onto model environmental surfaces. Water Res. 129, 231–239 (2018).

    Google Scholar 

  84. 84.

    Avena, M. J. & Koopal, L. K. Kinetics of humic acid adsorption at solid-water interfaces. Environ. Sci. Technol. 33, 2739–2744 (1999).

    Google Scholar 

  85. 85.

    Lee, S. S., Fenter, P., Park, C. & Nagy, K. L. Fulvic acid sorption on muscovite mica as a function of pH and time using in situ X-ray reflectivity. Langmuir 24, 7817–7829 (2008).

    Google Scholar 

  86. 86.

    Lilienfein, J., Qualls, R. G., Uselman, S. M. & Bridgham, S. D. Adsorption of dissolved organic carbon and nitrogen in soils of a weathering chronosequence. Soil Sci. Soc. Am. J. 68, 292–305 (2004).

    Google Scholar 

  87. 87.

    Mostovaya, A., Hawkes, J. A., Dittmar, T. & Tranvik, L. J. Molecular determinants of dissolved organic matter reactivity in lake water. Front. Earth Sci. 5, 106 (2017).

    Google Scholar 

  88. 88.

    Chacon, S. S. et al. Mineral surfaces as agents of environmental proteolysis: mechanisms and controls. Environ. Sci. Technol. 53, 3018–3026 (2019).

    Google Scholar 

  89. 89.

    Haas, K. L. & Franz, K. J. Application of metal coordination chemistry to explore and manipulate cell biology. Chem. Rev. 109, 4921–4960 (2009).

    Google Scholar 

  90. 90.

    Christl, I. & Kretzschmar, R. C-1s NEXAFS spectroscopy reveals chemical fractionation of humic acid by cation-induced coagulation. Environ. Sci. Technol. 41, 1915–1920 (2007).

    Google Scholar 

  91. 91.

    Edwards, D. C. & Myneni, S. C. B. Hard and soft X-ray absorption spectroscopic investigation of aqueous Fe(III)-hydroxamate siderophore complexes. J. Phys. Chem. A 109, 10249–10256 (2005).

    Google Scholar 

  92. 92.

    Radke, C. J. Gibbs adsorption equation for planar fluid–fluid interfaces: invariant formalism. Adv. Colloid Interface Sci. 222, 600–614 (2015).

    Google Scholar 

  93. 93.

    Schwertmann, U. Inhibitory effect of soil organic matter on the crystallization of amorphous ferric hydroxide. Nature 212, 645–646 (1966).

    Google Scholar 

  94. 94.

    Eusterhues, K. et al. Characterization of ferrihydrite-soil organic matter coprecipitates by X-ray diffraction and Mossbauer spectroscopy. Environ. Sci. Technol. 42, 7891–7897 (2008).

    Google Scholar 

  95. 95.

    Levard, C. et al. Structure and distribution of allophanes, imogolite and proto-imogolite in volcanic soils. Geoderma 183, 100–108 (2012).

    Google Scholar 

  96. 96.

    Chen, C. M., Kukkadapu, R. & Sparks, D. L. Influence of coprecipitated organic matter on Fe2+(aq)-catalyzed transformation of ferrihydrite: implications for carbon dynamics. Environ. Sci. Technol. 49, 10927–10936 (2015).

    Google Scholar 

  97. 97.

    Kaiser, K. & Zech, W. Release of natural organic matter sorbed to oxides and a subsoil. Soil Sci. Soc. Am. J. 63, 1157–1166 (1999).

    Google Scholar 

  98. 98.

    Oren, A. & Chefetz, B. Sorptive and desorptive fractionation of dissolved organic matter by mineral soil matrices. J. Environ. Qual. 41, 526–533 (2012).

    Google Scholar 

  99. 99.

    Lippold, H. & Lippmann-Pipke, J. Effect of humic matter on metal adsorption onto clay materials: testing the linear additive model. J. Contam. Hydrol. 109, 40–48 (2009).

    Google Scholar 

  100. 100.

    Eusterhues, K. et al. Reduction of ferrihydrite with adsorbed and coprecipitated organic matter: microbial reduction by Geobacter bremensis vs. abiotic reduction by Na-dithionite. Biogeosciences 11, 4953–4966 (2014).

    Google Scholar 

  101. 101.

    Eusterhues, K., Rumpel, C., Kleber, M. & Kogel-Knabner, I. Stabilisation of soil organic matter by interactions with minerals as revealed by mineral dissolution and oxidative degradation. Org. Geochem. 34, 1591–1600 (2003).

    Google Scholar 

  102. 102.

    Grybos, M., Davranche, M., Gruau, G. & Petitjean, P. Is trace metal release in wetland soils controlled by organic matter mobility or Fe-oxyhydroxides reduction? J. Colloid Interface Sci. 314, 490–501 (2007).

    Google Scholar 

  103. 103.

    Pan, W., Kan, J., Inamdar, S., Chen, C. & Sparks, D. Dissimilatory microbial iron reduction release DOC (dissolved organic carbon) from carbon-ferrihydrite association. Soil Biol. Biochem. 103, 232–240 (2016).

    Google Scholar 

  104. 104.

    Poggenburg, C., Mikutta, R., Schippers, A., Dohrmann, R. & Guggenberger, G. Impact of natural organic matter coatings on the microbial reduction of iron oxides. Geochim. Cosmochim. Acta 224, 223–248 (2018).

    Google Scholar 

  105. 105.

    Thompson, A., Chadwick, O. A., Boman, S. & Chorover, J. Colloid mobilization during soil iron redox oscillations. Environ. Sci. Technol. 40, 5743–5749 (2006).

    Google Scholar 

  106. 106.

    Collignon, C., Ranger, J. & Turpault, M. P. Seasonal dynamics of Al- and Fe-bearing secondary minerals in an acid forest soil: influence of Norway spruce roots (Picea abies (L.) Karst.). Eur. J. Soil Sci. 63, 592–602 (2012).

    Google Scholar 

  107. 107.

    Ochs, M., Brunner, I., Stumm, W. & Cosovic, B. Effect of root exudates and humic substances on weathering kinetics. Water Air Soil Pollut. 68, 213–229 (1993).

    Google Scholar 

  108. 108.

    Fang, L., Cao, Y., Huang, Q., Walker, S. L. & Cai, P. Reactions between bacterial exopolymers and goethite: a combined macroscopic and spectroscopic investigation. Water Res. 46, 5613–5620 (2012).

    Google Scholar 

  109. 109.

    Goyne, K. W., Chorover, J., Zimmerman, A. R., Komarneni, S. & Brantley, S. L. Influence of mesoporosity on the sorption of 2,4-dichlorophenoxyacetic acid onto alumina and silica. J. Colloid Interface Sci. 272, 10–20 (2004).

    Google Scholar 

  110. 110.

    Johnston, C. T., Premachandra, G. S., Szabo, T., Lok, J. & Schoonheydt, R. A. Interaction of biological molecules with clay minerals: a combined spectroscopic and sorption study of lysozyme on saponite. Langmuir 28, 611–619 (2012).

    Google Scholar 

  111. 111.

    Hunter, W. R. et al. Metabolism of mineral-sorbed organic matter and microbial lifestyles in fluvial ecosystems. Geophys. Res. Lett. 43, 1582–1588 (2016).

    Google Scholar 

  112. 112.

    McGhee, I., Sannino, F., Gianfreda, L. & Burns, R. G. Bioavailability of 2,4-D sorbed to a chlorite-like complex. Chemosphere 39, 285–291 (1999).

    Google Scholar 

  113. 113.

    Keiluweit, M. et al. Mineral protection of soil carbon counteracted by root exudates. Nat. Clim. Change 5, 588–595 (2015).

    Google Scholar 

  114. 114.

    Kallenbach, C. M., Frey, S. D. & Grandy, A. S. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat. Commun. 7, 13630 (2016).

    Google Scholar 

  115. 115.

    Malik, A. & Gleixner, G. Importance of microbial soil organic matter processing in dissolved organic carbon production. FEMS Microbiol. Ecol. 86, 139–148 (2013).

    Google Scholar 

  116. 116.

    Simpson, A. J., Simpson, M. J., Smith, E. & Kelleher, B. P. Microbially derived inputs to soil organic matter: are current estimates too low? Environ. Sci. Technol. 41, 8070–8076 (2007).

    Google Scholar 

  117. 117.

    Ferris, J. P. Montmorillonite catalysis of 30–50 mer oligonucleotides: laboratory demonstration of potential steps in the origin of the RNA world. Orig. Life Evol. Biosph. 32, 311–332 (2002).

    Google Scholar 

  118. 118.

    Aldersley, M. F., Joshi, P. C., Price, J. D. & Ferris, J. P. The role of montmorillonite in its catalysis of RNA synthesis. Appl. Clay Sci. 54, 1–14 (2011).

    Google Scholar 

  119. 119.

    Duval, S. et al. On the why’s and how’s of clay minerals’ importance in life’s emergence. Appl. Clay Sci. 195, 105737 (2020).

    Google Scholar 

  120. 120.

    Laszlo, P. Chemical reactions on clays. Science 235, 1473–1477 (1987).

    Google Scholar 

  121. 121.

    McBride, M. B. Adsorption and oxidation of phenolic compounds by iron and manganese oxides. Soil Sci. Soc. Am. J. 51, 1466–1472 (1987).

    Google Scholar 

  122. 122.

    Sheng, F. et al. Rapid hydrolysis of penicillin antibiotics mediated by adsorbed zinc on goethite surfaces. Environ. Sci. Technol. 53, 10705–10713 (2019).

    Google Scholar 

  123. 123.

    Chorover, J. & Amistadi, M. K. Reaction of forest floor organic matter at goethite, birnessite and smectite surfaces. Geochim. Cosmochim. Acta 65, 95–109 (2001).

    Google Scholar 

  124. 124.

    Faure, P., Schlepp, L., Burkle-Vitzthum, V. & Elie, M. Low temperature air oxidation of n-alkanes in the presence of Na-smectite. Fuel 82, 1751–1762 (2003).

    Google Scholar 

  125. 125.

    Mitchell, P. J. et al. Solution-state NMR investigation of the sorptive fractionation of dissolved organic matter by alkaline mineral soils. Environ. Chem. 10, 333–340 (2013).

    Google Scholar 

  126. 126.

    Riedel, T., Zak, D., Biester, H. & Dittmar, T. Iron traps terrestrially derived dissolved organic matter at redox interfaces. Proc. Natl Acad. Sci. USA 110, 10101–10105 (2013).

    Google Scholar 

  127. 127.

    Chacon, S. S., Garcia-Jaramillo, M., Liu, S. Y., Ahmed, M. & Kleber, M. Differential capacity of kaolinite and birnessite to protect surface associated proteins against thermal degradation. Soil Biol. Biochem. 119, 101–109 (2018).

    Google Scholar 

  128. 128.

    Reardon, P. N. et al. Abiotic protein fragmentation by manganese oxide: implications for a mechanism to supply soil biota with oligopeptides. Environ. Sci. Technol. 50, 3486–3493 (2016).

    Google Scholar 

  129. 129.

    Johnson, K. et al. Towards a mechanistic understanding of carbon stabilization in manganese oxides. Nat. Commun. 6, 7628 (2015).

    Google Scholar 

  130. 130.

    Cleaves, H. J. et al. Mineral–organic interfacial processes: potential roles in the origins of life. Chem. Soc. Rev. 41, 5502–5525 (2012).

    Google Scholar 

  131. 131.

    Soma, Y. & Soma, M. Chemical reactions of organic compounds on clay surfaces. Environ. Health Perspect. 83, 205–214 (1989).

    Google Scholar 

  132. 132.

    Norde, W. My voyage of discovery to proteins in flatland … and beyond. Colloids Surf. B Biointerfaces 61, 1–9 (2008).

    Google Scholar 

  133. 133.

    Hoarau, M., Badieyan, S. & Marsh, E. N. G. Immobilized enzymes: understanding enzyme–surface interactions at the molecular level. Org. Biomol. Chem. 15, 9539–9551 (2017).

    Google Scholar 

  134. 134.

    Maurice, P. A. & Namjesnik-Dejanovic, K. Aggregate structures of sorbed humic substances observed in aqueous solution. Environ. Sci. Technol. 33, 1538–1541 (1999).

    Google Scholar 

  135. 135.

    Myneni, S. C. B., Brown, J. T., Martinez, G. A. & Meyer-Ilse, W. Imaging of humic substance macromolecular structures in water and soils. Science 286, 1335–1337 (1999).

    Google Scholar 

  136. 136.

    Denton, J. K. et al. Molecular-level origin of the carboxylate head group response to divalent metal ion complexation at the air–water interface. Proc. Natl Acad. Sci. USA 116, 14874–14880 (2019).

    Google Scholar 

  137. 137.

    Liu, W., Tkatchenko, A. & Scheffler, M. Modeling adsorption and reactions of organic molecules at metal surfaces. Acc. Chem. Res. 47, 3369–3377 (2014).

    Google Scholar 

  138. 138.

    Nealson, K. H. & Saffarini, D. Iron and manganese in anaerobic respiration: Environmental significance, physiology, and regulation. Annu. Rev. Microbiol. 48, 311–343 (1994).

    Google Scholar 

  139. 139.

    Shi, L. et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14, 651–662 (2016).

    Google Scholar 

  140. 140.

    Gorby, Y. A. et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl Acad. Sci. USA 103, 11358–11363 (2006).

    Google Scholar 

  141. 141.

    Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098–1101 (2005).

    Google Scholar 

  142. 142.

    Marsili, E. et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc. Natl Acad. Sci. USA 105, 3968–3973 (2008).

    Google Scholar 

  143. 143.

    Remucal, C. K. & Ginder-Vogel, M. A critical review of the reactivity of manganese oxides with organic contaminants. Environ. Sci. Process. Impacts 16, 1247–1266 (2014).

    Google Scholar 

  144. 144.

    Sunda, W. G. & Kieber, D. J. Oxidation of humic substances by manganese oxides yields low-molecular weight organic substrates. Nature 367, 62–64 (1994).

    Google Scholar 

  145. 145.

    Ma, D., Wu, J., Yang, P. & Zhu, M. Q. Coupled manganese redox cycling and organic carbon degradation on mineral surfaces. Environ. Sci. Technol. 54, 8801–8810 (2020).

    Google Scholar 

  146. 146.

    Russo, F., Johnson, C. J., McKenzie, D., Aiken, J. M. & Pedersen, J. A. Pathogenic prion protein is degraded by a manganese oxide mineral found in soils. J. Gen. Virol. 90, 275–280 (2009).

    Google Scholar 

  147. 147.

    Heckman, K., Vazquez-Ortega, A., Gao, X. D., Chorover, J. & Rasmussen, C. Changes in water extractable organic matter during incubation of forest floor material in the presence of quartz, goethite and gibbsite surfaces. Geochim. Cosmochim. Acta 75, 4295–4309 (2011).

    Google Scholar 

  148. 148.

    Lehmann, R. G., Cheng, H. H. & Harsh, J. B. Oxidation of phenolic acids by soil iron and manganese oxides. Soil Sci. Soc. Am. J. 51, 352–356 (1987).

    Google Scholar 

  149. 149.

    Stuckey, J. W. et al. Impacts of hydrous manganese oxide on the retention and lability of dissolved organic matter. Geochem. Trans. 19, 6 (2018).

    Google Scholar 

  150. 150.

    Suter, D., Banwart, S. & Stumm, W. Dissolution of hydrous iron(III) oxides by reductive mechanisms. Langmuir 7, 809–813 (1991).

    Google Scholar 

  151. 151.

    Keiluweit, M. et al. Long-term litter decomposition controlled by manganese redox cycling. Proc. Natl Acad. Sci. USA 112, E5253–E5260 (2015).

    Google Scholar 

  152. 152.

    Jones, M. E. et al. Manganese-driven carbon oxidation at oxic-anoxic interfaces. Environ. Sci. Technol. 52, 12349–12357 (2018).

    Google Scholar 

  153. 153.

    Estes, E. R., Andeer, P. F., Nordlund, D., Wankel, S. & Hansel, C. M. Biogenic manganese oxides as reservoirs of organic carbon and proteins in terrestrial and marine environments. Geobiology 15, 158–172 (2016).

    Google Scholar 

  154. 154.

    Fridovich, I. Oxygen toxicity: a radical explanation. J. Exp. Biol. 201, 1203–1209 (1998).

    Google Scholar 

  155. 155.

    Trusiak, A., Treibergs, L. A., Kling, G. W. & Cory, R. M. The role of iron and reactive oxygen species in the production of CO2 in arctic soil waters. Geochim. Cosmochim. Acta 224, 80–95 (2018).

    Google Scholar 

  156. 156.

    Hansel, C. M. & Diaz, J. M. Production of extracellular reactive oxygen species by marine biota. Annu. Rev. Mar. Sci. 13, 177–200 (2021).

    Google Scholar 

  157. 157.

    Blough, N. V. & Zepp, R. G. in Active Oxygen in Chemistry (eds Foote, C. S., Valentine, J. S., Greenburg, A., & Liebman, J. F.) 280–333 (Blackie Academic, 1995).

  158. 158.

    Xu, X. et al. Characteristics of desert varnish from nanometer to micrometer scale: A photo-oxidation model on its formation. Chem. Geol. 522, 55–70 (2019).

    Google Scholar 

  159. 159.

    Schoonen, M. A. A. et al. in Medical Mineralogy and Geochemistry (eds Sahia, N., Schoonen, M. A. A., & Skinner, H. C. W.) 59–113 (Mineralogical Society of America, 2006).

  160. 160.

    Georgiou, C. D. et al. Evidence for photochemical production of reactive oxygen species in desert soils. Nat. Commun. 6, 7100 (2015).

    Google Scholar 

  161. 161.

    Gil-Lozano, C., Davila, A. F., Losa-Adams, E., Fairen, A. G. & Gago-Duport, L. Quantifying Fenton reaction pathways driven by self-generated H2O2 on pyrite surfaces. Sci. Rep. 7, 43703 (2017).

    Google Scholar 

  162. 162.

    Tong, M. et al. Production of abundant hydroxyl radicals from oxygenation of subsurface sediments. Environ. Sci. Technol. 50, 214–221 (2016).

    Google Scholar 

  163. 163.

    Xu, J., Sahia, N., Eggleston, C. M. & Schoonen, M. A. A. Reactive oxygen species at the oxide/water interface: Formation mechanisms and implications for prebiotic chemistry and the origin of life. Earth Planet Sci. Lett. 363, 156–167 (2013).

    Google Scholar 

  164. 164.

    Yuan, X. et al. Production of hydrogen peroxide in groundwater at Rifle, Colorado. Environ. Sci. Technol. 51, 7881–7891 (2017).

    Google Scholar 

  165. 165.

    Sutherland, K. M. et al. Spatial heterogeneity in particle-associated, light-independent superoxide production within productive coastal waters. J. Geophys. Res. Oceans 125, e2020JC016747 (2020).

    Google Scholar 

  166. 166.

    Page, S. E. et al. Dark formation of hydroxyl radical in arctic soil and surface waters. Environ. Sci. Technol. 47, 12860–12867 (2013).

    Google Scholar 

  167. 167.

    Rose, A. L. The influence of extracellular superoxide on iron redox chemistry and bioavailability to aquatic microorganisms. Front Microbiol. 3, 124 (2012).

    Google Scholar 

  168. 168.

    Waggoner, D. C., Wozniak, A. S., Cory, R. M. & Hatcher, P. G. The role of reactive oxygen species in the degradation of lignin derived dissolved organic matter. Geochim. Cosmochim. Acta 208, 171–184 (2017).

    Google Scholar 

  169. 169.

    Goldstone, J. V. & Voelker, B. M. Chemistry of superoxide radical in seawater: CDOM associated sink of superoxide in coastal waters. Environ. Sci. Technol. 34, 1043–1048 (2000).

    Google Scholar 

  170. 170.

    Voelker, B. M. & Sulzberger, B. Effects of fulvic acid on Fe(II) oxidation by hydrogen peroxide. Environ. Sci. Technol. 30, 1106–1114 (1996).

    Google Scholar 

  171. 171.

    Buxton, G. V., Greenstock, C. L., Helman, W. P. & Ross, A. B. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (OH/O) in aqueous solution. J. Phys. Chem. Ref. Data 17, 513–886 (1988).

    Google Scholar 

  172. 172.

    Goldstone, J. V., Pullin, M. J., Bertilsson, S. & Voelker, B. M. Reactions of hydroxyl radical with humic substances: bleaching, mineralization, and production of bioavailable carbon substrates. Environ. Sci. Technol. 36, 364–372 (2002).

    Google Scholar 

  173. 173.

    Pullin, M. J., Bertilsson, S., Goldstone, J. V. & Voelker, B. M. Effects of sunlight and hydroxyl radical on dissolved organic matter: Bacterial growth efficiency and production of carboxylic acids and other substrates. Limnol. Oceanogr. 49, 2011–2022 (2014).

    Google Scholar 

  174. 174.

    Wuttig, K., Heller, M. I. & Croot, P. L. Pathways of superoxide (O2) decay in the eastern Tropical North Atlantic. Environ. Sci. Technol. 47, 10249–10256 (2013).

    Google Scholar 

  175. 175.

    Heller, M. I., Wuttig, K. & Croot, P. L. Identifying the sources and sinks of CDOM/FDOM across the Mauritanian Shelf and their potential role in the decomposition of superoxide (O2-). Front. Mar. Sci. 3, 132 (2016).

    Google Scholar 

  176. 176.

    Scully, N. M., Cooper, W. J. & Tranvik, L. J. Photochemical effects on microbial activity in natural waters: the interaction of reactive oxygen species and dissolved organic matter. FEMS Microbiol. Ecol. 46, 353–357 (2003).

    Google Scholar 

  177. 177.

    Hall, S. J. & Silver, W. L. Iron oxidation stimulates organic matter decomposition in humid tropical forest soils. Glob. Change Biol. 19, 2804–2813 (2013).

    Google Scholar 

  178. 178.

    Xiao, Y. H., Carena, L., Näsi, M.-T. & Vähätalo, A. V. Superoxide-driven autocatalytic dark production of hydroxyl radicals in the presence of complexes of natural dissolved organic matter and iron. Water Res. 177, 115782 (2020).

    Google Scholar 

  179. 179.

    Bach, C. E. et al. Measuring phenol oxidase and peroxidase activities with pyrogallol, L-DOPA, and ABTS: effect of assay conditions and soil type. Soil Biol. Biochem. 67, 183–191 (2013).

    Google Scholar 

  180. 180.

    Carson, J. K. et al. Low pore connectivity increases bacterial diversity in soil. Appl. Environ. Microbiol. 76, 3936–3942 (2010).

    Google Scholar 

  181. 181.

    Negassa, W. C. et al. Properties of soil pore space regulate pathways of plant residue decomposition and community structure of associated bacteria. PLoS ONE 10, e0123999 (2015).

    Google Scholar 

  182. 182.

    Keiluweit, M., Gee, K., Denney, A. & Fendorf, S. Anoxic microsites in upland soils dominantly controlled by clay content. Soil Biol. Biochem. 118, 42–50 (2018).

    Google Scholar 

  183. 183.

    Sexstone, A. J., Revsbech, N. P., Parkin, T. B. & Tiedje, J. M. Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci. Soc. Am. J. 49, 645–651 (1985).

    Google Scholar 

  184. 184.

    Treves, D. S., Xia, B., Zhou, J. & Tiedje, J. M. A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Microb. Ecol. 45, 20–28 (2003).

    Google Scholar 

  185. 185.

    Estes, E. R. et al. Persistent organic matter in oxic subseafloor sediment. Nat. Geosci. 12, 126–131 (2019).

    Google Scholar 

  186. 186.

    Nunan, N. The microbial habitat in soil: scale, heterogeneity and functional consequences. J. Plant. Nutr. Soil Sci. 180, 425–429 (2017).

    Google Scholar 

  187. 187.

    Crawford, J. W., Harris, J. A., Ritz, K. & Young, I. M. Towards an evolutionary ecology of life in soil. Trends Ecol. Evol. 20, 81–87 (2005).

    Google Scholar 

  188. 188.

    Dignac, M.-F. et al. Increasing soil carbon storage: mechanisms, effects of agricultural practices and proxies. A review. Agron Sustain Dev 37, 14 (2017).

    Google Scholar 

  189. 189.

    Rawlins, B. G. et al. Three-dimensional soil organic matter distribution, accessibility and microbial respiration in macroaggregates using osmium staining and synchrotron X-ray computed tomography. SOIL 2, 659–671 (2016).

    Google Scholar 

  190. 190.

    Raynaud, X. & Nunan, N. Spatial ecology of bacteria at the microscale in soil. PLoS ONE (2014).

    Article  Google Scholar 

  191. 191.

    Kuzyakov, Y. & Blagodatskaya, E. Microbial hotspots and hot moments in soil: concept & review. Soil Biol. Biochem. 83, 184–199 (2015).

    Google Scholar 

  192. 192.

    Shi, A. et al. Substrate spatial heterogeneity reduces soil microbial activity. Soil Biol. Biochem. 152, 108068 (2021).

    Google Scholar 

  193. 193.

    Rillig, M. C., Muller, L. A. H. & Lehmann, A. Soil aggregates as massively concurrent evolutionary incubators. ISME J. 11, 1943–1948 (2017).

    Google Scholar 

  194. 194.

    Wilpiszeski, R. L. et al. Soil aggregate microbial communities: towards understanding microbiome interactions at biologically relevant scales. Appl. Environ. Microbiol. 85, e00324–19 (2019).

    Google Scholar 

  195. 195.

    Philippot, L. et al. Dissimilatory nitrite-reductase provides a competitive advantage to Pseudomonas sp. RTC01 to colonise the centre of soil aggregates. FEMS Microbiol. Ecol. 21,175–185 (1996).

    Google Scholar 

  196. 196.

    Kuo, C. H., Moran, N. A. & Ochman, H. The consequences of genetic drift for bacterial genome complexity. Genome Res. 19, 1450–1454 (2009).

    Google Scholar 

  197. 197.

    Chenu, C. & Stotzky, G. in Interactions between Soil Particles and Microorganisms (eds Huang, P. M., Bollag, J.-M. & Senesi, N.) (Wiley, 2002).

  198. 198.

    Uroz, S., Kelly, L. C., Turpault, M. P., Lepleux, C. & Frey-Klett, P. The mineralosphere concept: mineralogical control of the distribution and function of mineral-associatec bacterial communities. Trends Microbiol. 23, 751–762 (2015).

    Google Scholar 

  199. 199.

    Marlow, J. J. et al. Microbial abundance and diversity patterns associated with sediments and carbonates from the methane seep environments of Hydrate Ridge, OR. Front. Mar. Sci. (2014).

    Article  Google Scholar 

  200. 200.

    Vieira, S. et al. Bacterial colonization of minerals in grassland soils is selective and highly dynamic. Environ. Microbiol. 22, 917–933 (2019).

    Google Scholar 

  201. 201.

    Whitman, T. et al. Microbial community assembly differs across minerals in a rhizosphere microcosm. Environ. Microbiol. 20, 4444–4460 (2018).

    Google Scholar 

  202. 202.

    Ahmed, E. et al. Mineral type structures soil microbial communities. Geomicrobiol. J. 34, 538–545 (2017).

    Google Scholar 

  203. 203.

    Newman, D. K. How bacteria respire minerals. Science 292, 1312–1313 (2001).

    Google Scholar 

  204. 204.

    Filip, Z. Clay minerals as a factor influencing the biochemical activity of soil microorganisms. Folia Microbiol. 18, 56–74 (1973).

    Google Scholar 

  205. 205.

    Cai, P. et al. Impact of soil clay minerals on growth, biofilm formation, and virulence gene expression of Escherichia coli O157:H7. Environ. Pollut. 243, 953–960 (2018).

    Google Scholar 

  206. 206.

    Huayong Wu, H. et al. Soil colloids and minerals modulate metabolic activity of measured using microcalorimetry. Geomicrobiol. J. 31, 590–596 (2014).

    Google Scholar 

  207. 207.

    Stotzky, G. & Rem, L. T. Influence of clay minerals on microorganisms. I. Montmorillonite and kaolinite on bacteria. Can. J. Microbiol. 12, 547–563 (1966).

    Google Scholar 

  208. 208.

    Stotzky, G. & Rem, L. T. Influence of clay minerals on microorganisms. IV. Montmorillonite and kaolinites on fungi. Can. J. Microbiol. 13, 1535–1550 (1967).

    Google Scholar 

  209. 209.

    Miltner, A., Bombach, P., Schmidt-Brucken, B. & Kastner, M. SOM genesis: microbial biomass as a significant source. Biogeochemistry 111, 41–55 (2012).

    Google Scholar 

  210. 210.

    Francesca Cotrufo, M. et al. Formation of soil organic matter via biochemical and physical pathways of litter mass loss. Nat. Geosci. 8, 776–779 (2015).

    Google Scholar 

  211. 211.

    Angst, G., Mueller, K. E., Nierop, K. G. J. & Simpson, M. J. Plant- or microbial-derived? A review on the molecular composition of stabilized soil organic matter. Soil Biol. Biochem. 156, 108189 (2021).

    Google Scholar 

  212. 212.

    Liang, C., Amelung, W., Lehmann, J. & Kastner, M. Quantitative assessment of microbial necromass contribution to soil organic matter. Glob. Change Biol. 25, 3578–3590 (2019).

    Google Scholar 

  213. 213.

    Sokol, N. W. & Bradford, M. A. Microbial formation of stable soil carbon is more efficient from belowground than aboveground input. Nat. Geosci. 12, 46–53 (2019).

    Google Scholar 

  214. 214.

    Young, I. M. & Crawford, J. W. Interactions and self-organization in the soil-microbe complex. Science 304, 1634–1637 (2004).

    Google Scholar 

  215. 215.

    Levin, S. A. Ecosystems and the biosphere as complex adaptive systems. Ecosystems 1, 431–436 (1998).

    Google Scholar 

  216. 216.

    D’Souza, G. et al. Less is more: selective advantages can explain the prevalent loss of biosynthetic genes in bacteria. Evolution 68, 2559–2570 (2014).

    Google Scholar 

  217. 217.

    Pascual-Garcia, A., Bonhoeffer, S. & Bell, T. Metabolically cohesive microbial consortia and ecosystem functioning. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190245 (2020).

    Google Scholar 

  218. 218.

    Pande, S. & Kost, C. Bacterial unculturability and the formation of intercellular metabolic networks. Trends Microbiol. 25, 349–361 (2017).

    Google Scholar 

  219. 219.

    D’Souza, G. & Kost, C. Experimental evolution of metabolic dependency in bacteria. PLoS Genetics 12, e1006364 (2016).

    Google Scholar 

  220. 220.

    Six, J., Elliott, E. T. & Paustian, K. Soil structure and soil organic matter: II. A normalized stability index and the effect of mineralogy. Soil. Sci. Soc. Am. J. 64, 1042–1049 (2000).

    Google Scholar 

  221. 221.

    Denef, K., Six, J., Merckx, R. & Paustian, K. Short-term effects of biological and physical forces on aggregate formation in soils with different clay mineralogy. Plant Soil 246, 185–200 (2002).

    Google Scholar 

  222. 222.

    Lehmann, J. et al. Persistence of soil organic carbon caused by functional complexity. Nat. Geosci. 13, 529–534 (2020).

    Google Scholar 

  223. 223.

    Nunan, N., Schmidt, H. & Raynaud, X. The ecology of heterogeneity: soil bacterial communities and C dynamics. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190249 (2020).

    Google Scholar 

  224. 224.

    Wilhelm, R. C., Pepe-Ranney, C., Weisenhorn, P., Lipton, M. & Buckley, D. H. Competitive exclusion and metabolic dependency among microorganisms structure the cellulose economy of an agricultural soil. mBio (2021).

    Article  Google Scholar 

  225. 225.

    Kalbitz, K., Schwesig, D., Rethemeyer, J. & Matzner, E. Stabilization of dissolved organic matter by sorption to the mineral soil. Soil Biol. Biochem. 37, 1319–1331 (2005).

    Google Scholar 

  226. 226.

    Zhalnina, K. et al. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat. Microbiol. 3, 470–480 (2018).

    Google Scholar 

  227. 227.

    Woolf, D. & Lehmann, J. Microbial models with minimal mineral protection can explain long-term soil organic carbon persistence. Sci. Rep. 9, 6522 (2019).

    Google Scholar 

  228. 228.

    Borer, B., Tecon, R. & Or, D. Spatial organization of bacterial populations in response to oxygen and carbon counter-gradients in pore networks. Nat. Commun. 9, 769 (2018).

    Google Scholar 

  229. 229.

    Barzen-Hanson, K. A., Davis, S. E., Kleber, M. & Field, J. A. Sorption of fluorotelomer sulfonates, fluorotelomer sulfonamido betaines, and a fluorotelomer sulfonamido amine in national foam aqueous film-forming foam to soil. Environ. Sci. Technol. 51, 12394–12404 (2017).

    Google Scholar 

  230. 230.

    Grabowski, R. C., Droppo, I. G. & Wharton, G. Erodibility of cohesive sediment: The importance of sediment properties. Earth Sci. Rev. 105, 101–120 (2011).

    Google Scholar 

  231. 231.

    Shen, X. Y. & Bourg, I. C. Molecular dynamics simulations of the colloidal interaction between smectite clay nanoparticles in liquid water. J. Colloid Interface Sci. 584, 610–621 (2021).

    Google Scholar 

  232. 232.

    Israelachvili, J. & Wennerstrom, H. Role of hydration and water structure in biological and colloidal interactions. Nature 379, 219–225 (1996).

    Google Scholar 

  233. 233.

    Sushko, M. L. & Rosso, K. M. The origin of facet selectivity and alignment in anatase TiO2 nanoparticles in electrolyte solutions: implications for oriented attachment in metal oxides. Nanoscale 8, 19714–19725 (2016).

    Google Scholar 

  234. 234.

    Michot, L. J. et al. Liquid-crystalline aqueous clay suspensions. Proc. Natl Acad. Sci. USA 103, 16101–16104 (2006).

    Google Scholar 

  235. 235.

    Underwood, T. R. & Bourg, I. C. Large-scale molecular dynamics simulation of the dehydration of a suspension of smectite clay nanoparticles. J. Phys. Chem. C 124, 3702–3714 (2020).

    Google Scholar 

  236. 236.

    Pignon, F. et al. Yield stress thixotropic clay suspension: Investigation of structure by light, neutron, and X-ray scattering. Phys. Rev. E 56, 3281–3289 (1997).

    Google Scholar 

  237. 237.

    Bourg, I. C. & Ajo-Franklin, J. B. Clay, water, and salt: controls on the permeability of fine-grained sedimentary rocks. Acc. Chem. Res. 50, 2067–2074 (2017).

    Google Scholar 

  238. 238.

    Mayer, L. M. Surface area control of organic carbon accumulation in continental shelf sediments. Geochim. Cosmochim. Acta 58, 1271–1284 (1994).

    Google Scholar 

  239. 239.

    Ransom, B., Dongsom, K., Kastner, M. & Wainwright, S. Organic matter preservation on continental slopes: Importance of mineralogy and surface area. Geochim. Cosmochim. Acta 62, 1329–1345 (1998).

    Google Scholar 

  240. 240.

    Kaiser, K. & Guggenberger, G. Mineral surfaces and soil organic matter. Eur. J. Soil Sci. 54, 219–236 (2003).

    Google Scholar 

  241. 241.

    Barker, W. W., Welch, S. A., Chu, S. & Banfield, J. F. Experimental observations of the effects of bacteria on aluminosilicate weathering. Am. Mineral. 83, 1551–1563 (1998).

    Google Scholar 

  242. 242.

    Watteau, F. & Villemin, G. Soil microstructures examined through transmission electron microscopy reveal soil-microorganisms interactions. Front. Environ. Sci. 6, 106 (2018).

    Google Scholar 

  243. 243.

    Namjesnik-Dejanovic, K. & Maurice, P. A. Conformations and aggregate structures of sorbed natural organic matter on muscovite and hematite. Geochim. Cosmochim. Acta 65, 1047–1057 (2001).

    Google Scholar 

  244. 244.

    Moreau, J. W. et al. Extracellular proteins limit the dispersal of biogenic nanoparticles. Science 316, 1600–1603 (2007).

    Google Scholar 

  245. 245.

    Jaynes, W. F. & Boyd, S. A. Hydrophobicity of siloxane surfaces in smectites as revealed by aromatic hydrocarbon adsorption from water. Clays Clay Miner. 39, 428–436 (1991).

    Google Scholar 

  246. 246.

    Rotenberg, B., Patel, A. J. & Chandler, D. Molecular explanation for why talc surfaces can be both hydrophilic and hydrophobic. J. Am. Chem. Soc. 133, 20521–20527 (2011).

    Google Scholar 

  247. 247.

    Radke, C. J. & Prausnitz, J. M. Thermodynamics of multi-solute adsorption from dilute liquid solutions. AIChe J. 18, 761–768 (1972).

    Google Scholar 

  248. 248.

    Degennes, P. G. Wetting: statics and dynamics. Rev. Mod. Phys. 57, 827–863 (1985).

    Google Scholar 

  249. 249.

    McGinley, P. M., Katz, L. E. & Weber, W. J. A distributed reactivity model for sorption by soils and sediments. 2. Multicomponent systems and competitive effects. Environ. Sci. Technol. 27, 1524–1531 (1993).

    Google Scholar 

  250. 250.

    Davey, M. E., Caiazza, N. C. & O’Toole, G. A. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185, 1027–1036 (2003).

    Google Scholar 

  251. 251.

    Zhang, Y. M. & Miller, R. M. Enhanced octadecane dispersion and biodegradation by a Pseudomonas rhamnolipid surfactant (biosurfactant). Appl. Environ. Microbiol. 58, 3276–3282 (1992).

    Google Scholar 

  252. 252.

    Myneni, S. C. B. Chemistry of natural organic matter — The next step: Commentary on a humic substances debate. J. Environ. Qual. 48, 233–235 (2019).

    Google Scholar 

  253. 253.

    Kleber, M. & Lehmann, J. Humic substances extracted by alkali are invalid proxies for the dynamics and functions of organic matter in terrestrial and aquatic ecosystems. J. Environ. Qual. 48, 207–216 (2019).

    Google Scholar 

  254. 254.

    Hazen, R. M. & Sverjensky, D. A. Mineral surfaces, geochemical complexities, and the origins of life. Cold Spring Harb. Perspect. Biol. 2, a002162 (2010).

    Google Scholar 

  255. 255.

    Huang, P. M. & Hardie, A. G. in Biophysico-Chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems (eds Senesi, N., Xing, B., & Huang, P. M.) 41–109 (Wiley, 2009).

  256. 256.

    Huang, P. M. & Hardie, A. G. in Handbook of Soil Sciences: Properties and Processes (eds Huang, P. M., Li, Y., & Sumner, M. E.) 18.11–18.40 (CRC Press, 2012).

  257. 257.

    Van Loosdrecht, M. C. M., Lyklema, J., Norde, W. & Zehnder, A. J. B. Influence of interfaces on microbial activity. Microbiol. Rev. 54, 75–87 (1990).

    Google Scholar 

  258. 258.

    Lipson, D. A., Jha, M., Raab, T. K. & Oechel, W. C. Reduction of iron(III) and humic substances plays a major role in anaerobic respiration in an Arctic peat soil. J. Geophys. Res. Biogeosci. 115, G00I06 (2010).

    Google Scholar 

  259. 259.

    Paerl, R. W., Claudio, I. M., Shields, M. R., Bianchi, T. S. & Osburn, C. L. Dityrosine formation via reactive oxygen consumption yields increasingly recalcitrant humic-like fluorescent organic matter in the ocean. Limnol. Oceanogr. Lett. 5, 337–345 (2020).

    Google Scholar 

  260. 260.

    Guggenheim, S. et al. Summary of recommendations of nomenclature committees relevant to clay mineralogy: Report of the Association Internationale pour l’Etude des Argiles (AIPEA) Nomenclature Committee for 2006. Clays Clay Miner. 54, 761–772 (2006).

    Google Scholar 

  261. 261.

    Theng, B. K. G. & Yuan, G. Nanoparticles in the soil environment. Elements 4, 395–399 (2008).

    Google Scholar 

  262. 262.

    Tournassat, C., Bourg, I. C., Steefel, C. I. & Bergaya, F. in Developments in Clay Science Vol. 6 (eds Tournassat, C., Steefel, C. I., Bourg, I. C., & Bergaya, F.) 5–31 (Elsevier, 2015).

  263. 263.

    Hansel, C. M. et al. Secondary mineralization pathways induced by dissimilatory iron reduction of ferrihydrite under advective flow. Geochim. Cosmochim. Acta 67, 2977–2992 (2003).

    Google Scholar 

  264. 264.

    Biesgen, D., Frindte, K., Maarastawi, S. & Knief, C. Clay content modulates differences in bacterial community structure in soil aggregates of different size. Geoderma 376, 114544 (2020).

    Google Scholar 

Download references


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.

Author information




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.

Corresponding author

Correspondence to Markus Kleber.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information

Nature Reviews Earth & Environment thanks M. Aeppli, L. Aristilde and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.



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.


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• −).


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


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


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


The ability to derive nutritional requirements from complex organic substances.


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.


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).


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).


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.


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.


The process by which nuclei are formed in solution.


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.


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.


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


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


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


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


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).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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).

Download citation


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing