Competition within low-density bacterial populations as an unexpected factor regulating carbon decomposition in bulk soil

Abstract

Bacterial decomposition of organic matter in soils is generally believed to be mainly controlled by the accessibility of bacteria to their substrate. The influence of bacterial metabolic traits on this control has however received little attention in highly heterogeneous spatial conditions under advective-dispersive transport of bacteria and substrates. Here, we develop a biochemical transport model to screen the interactive impacts of dispersion and metabolic traits on mineralization. We compare the model results with two sets of previously performed cm-scale soil-core experiments in which the mineralization of the pesticide 2,4-D was measured under well-controlled initial distributions and transport conditions. Bacterial dispersion away from the source of substrate induced a significant increase in 2,4-D mineralization, revealing the existence of a control of decomposition by the bacterial density, in addition to the accessibility to the substrate. This regulation of degradation by density becomes dominant for bacteria with an efficient uptake of substrate at low substrate concentrations (i.e. oligotrophs). The model output suggests that the distance between bacteria adapted to oligotrophic environments is a stronger regulator of degradation than the distance between substrate source and these bacteria. Such oligotrophs, commonly found in soils, compete with each other for substrate even under remarkably low population densities. The ratio-dependent Contois growth model, which includes a density regulation in the expression of the uptake efficiency, appears more versatile and accurate than the substrate-dependent Monod model. In view of their strong interactions, biochemical and transport processes cannot be handled independently but should be integrated, in particular when biochemical processes of interest are carried out by oligotrophs.Abstract FigureHighlights–Biodegradation in soils results from strong biochemical and transport couplings–Biodegradation depends on bacterial density, in addition to substrate accessibility–Bacterial density regulation counterbalances substrate accessibility regulation–Density regulation is enhanced for oligotrophic bacteria–The ratio-dependent Contois model is relevant to represent this double regulation

Biodegradation of Pesticides at the Limit: Kinetics and Microbial Substrate Use at Low Concentrations

“…Fundamentally different preconditions influence microbial degradation at low pesticide concentrations. When pesticide concentrations are low, the distance between the molecule and the microorganisms increases, minimizing the probability of contact ( Coche et al, 2018 ). Degradation of low pesticide concentrations often follows first-order kinetics ( Jacobsen and Pederson, 1992 ; Helweg et al, 1998 ) without microbial uptake as an energy or carbon source ( Fomsgaard and Kristensen, 1999 ).…”