The influence of structural complexity of microbial habitats on soil organic matter decomposition: a theoretical analysis

The soil pore space constitutes a highly heterogeneous habitat that harbors a rich microbial diversity. Microbial processes within soils are intricately linked to the physical and chemical characteristics of micro-environments of pores where they reside. The dynamics of decomposition of organic matter therefore is shaped by the dispersion dynamics or spatial constraints imposed on microorganisms and their enzymes. Therefore, incorporating the complex soil architecture into computational models at the microscale is a crucial step to improve our predictions of the dynamics of soil organic matter (SOM) turnover.

In this work, we employ theoretical models to elucidate the impact of soil structural complexity and heterogeneity on organic matter decomposition dynamics, and characterize mechanisms that enhance or constrain it. In the first part, we show the impact of compartmentalization of the substrate on enzyme activity, considering a scenario where microbes have no direct physical access to the substrate and only smaller freely diffusing enzymes can reach it. Our findings reveal that, in this context, enzyme lifetime imposes limitations on the turnover rate of the reaction, subsequently affecting the uptake and growth rates of microorganisms. In the second part, we examine the effect of soil architecture on microbial decomposition dynamics. Our results highlight two contrasting aspects necessary for rapid decomposition: on one hand there is a need for refuges/shelters where microbial activity is boosted trough accumulation of enzymes, and on the other there is a need for high connectivity (accessibility) of the pore space for the microbial population to spread. Through our examination, we unveil the intricate interplay between these apparently conflicting conditions and their profound effects on population growth and substrate decomposition rates.