The millimetre-scale distribution of 2,4-D and its degraders drives the fate of 2,4-D at the soil core scale

The biodegradation of organic compounds in soil is a key process that has major implications for different ecosystem services such as soil fertility, air and water quality, and climate regulation. Due to the complexity of soil, the distributions of organic compounds and microorganisms are heterogeneous on sub-cm scales, and biodegradation is therefore partly controlled by the respective localizations of organic substrates and degraders. If they are not co-localized, transfer processes become crucial for the accessibility and availability of the substrate to degraders. This spatial interaction is still poorly understood, leading to poor predictions of organic compound dynamics in soils. The objectives of this work were to better understand how the mm-scale distribution of a model pesticide, 2,4-dichlorophenoxyacetic acid (2,4-D), and its degraders drives the fate of 2,4-D at the cm soil core scale. We constructed cm-scale soil cores combining sterilized and “natural” soil aggregates in which we controlled the initial distributions of 2,4-D and soil microorganisms with the following spatial distributions: i) a homogeneous distribution of microorganisms and 2,4-D at the core-scale, ii) a co-localized distribution of microorganisms and 2,4-D in a single spot (360 mm³) and iii) a disjoint localization of microorganisms and 2,4-D in 2 soil spots (360 mm³) separated by 2 cm. Two sets of experiments were performed: one used radiolabeled ¹⁴C-2,4-D to study the fate of 2,4-D, and the other used ¹²C-2,4-D to follow the dynamics of degraders. Microcosms were incubated at 20 °C and at field capacity (?31.6 kPa). At the core scale, we followed 2,4-D mineralization over time. On three dates, soil cores with microorganisms and 2,4-D localized in soil spots, were cut out in slices and then in 360 mm³ soil cubes. The individual soil cubes were then independently analysed for extractable and non-extractable ¹⁴C and for degraders (quantitative PCR of tfdA genes). Knowing the initial position of each soil cube allowed us to establish 3D maps of 2,4-D residues and degraders in soil. The results indicated that microorganisms and pesticide localizations in soil are major driving factors of i) pesticide biodegradation, by regulating the accessibility of 2,4-D to degrading microorganisms (by diffusion); and ii) the formation of non-extractable residues (NER). These results also emphasized the dominant role of microorganisms in the formation and localization of biogenic NER at a mm-scale. To conclude, these results demonstrate the importance of considering micro-scale processes to better understand the fate of pesticides and more generally of soil organic substrates at upper scales in soil and suggest that such spatial heterogeneity should not be neglected when predicting the fate of organic compounds in soils.