Substrate spatial heterogeneity reduces soil microbial activity

Andong Shi,Arjun Chakrawal,Stefano Manzoni,Benjamin M.C Fischer,Naoise Nunan,Anke M Herrmann

doi:10.1016/j.soilbio.2020.108068

Abstract

Soil heterogeneity influences microbial access to substrates and creates habitats varying in substrate concentrations, thus leading to local variations in carbon (C) dynamics. Based on theoretical considerations, we expected that higher heterogeneity would decrease microbial activity. To test this hypothesis, we modified substrate spatial heterogeneity using 3D-printed cylinders with four compartments (either preventing or allowing diffusion between compartments). The same total amount of glucose (1.5 mg glucose C per cylinder) was added either to one compartment (highest local concentration, 2.0 mg glucose C g−1 soil, and highest heterogeneity), to two (medium concentration, 1.0 mg glucose C g−1 soil, and intermediate heterogeneity), or to four compartments (lowest local concentration, 0.5 mg glucose C g−1 soil, and equivalent to homogeneous conditions). Thus, we experimentally created a gradient of substrate spatial heterogeneity. The 3D cylinders containing soil were transferred into standard calorimetry ampoules and were incubated in isothermal calorimeters to monitor soil heat dissipation rates as a proxy of soil microbial activity over 51 h at 18 °C. When diffusion among compartments was prevented, the most heterogeneous treatment showed the lowest heat dissipation rates, despite having the highest local substrate concentration. Compared to homogeneous conditions, the heat dissipation rate from the most heterogeneous treatment was 110% lower at the beginning of the experiment (12.7 μJ g−1 soil s−1) and 50% lower when heat dissipation rates reached a peak (72.6 μJ g−1 soil s−1). Moreover, the peak was delayed by approximately 2 h compared to the most homogeneous treatment. When diffusion among compartments was allowed, the effect of substrate spatial heterogeneity on microbial activity was strongly diminished. Our findings emphasize the influence of substrate spatial heterogeneity on soil microbial dynamics, highlighting the importance of including it in C cycling models for a better understanding of soil C dynamics.

Highlights

Soil microbial communities are critical players in regulating soil C fluxes and the associated feedbacks to the climate system (Phillips and Nickerson, 2015)
The soil heat dissipation rate was at 26.6 ± 1.9 μJ g− 1 soil s− 1 in the 25-25-25-25% treatment at the beginning of the experiment (t = 3 h, when the heat signals were stabilized), which was between 67% and more than twice as much as the other treatments (Fig. 2a)
Soil microbial activity decreased with increasing degree of substrate spatial heterogeneity and the most heterogeneous treatment delayed the peak of microbial activity, compared to the homogeneous treatment

Summary

Introduction

Soil microbial communities are critical players in regulating soil C fluxes and the associated feedbacks to the climate system (Phillips and Nickerson, 2015). Pinheiro et al (2015) found that the co-localization of microbial de composers and pesticide 2,4-dichlorophenoxyaectic acid (2,4-D) played a critical role in regulating its degradation, and simulations showed a decrease in the degradation rate of 2,4-D with increasing distance be tween decomposer and substrate (Babey et al, 2017). These findings imply that substrates should be in the vicinity of microbial cells for the latter to successfully take them up, decompose or convert them into biomass (Pallud et al, 2004; Lehmann et al, 2020). The in fluence of substrate accessibility on microbial decomposition has been studied, we still do not know how accessibility combined with other factors, such as substrate concentration, affects microbial activity

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