Effect of pore network architecture on the efficiency of microbial soil organic matter decomposition

Abstract

Microbial decomposition of soil organic matter is one of the major drivers of nutrient and carbon cycling in terrestrial ecosystems. Soils are spatially heterogeneous habitats built up hierarchically from µm- to mm-sized aggregates that provide a complex pore system. An enormous diversity of microbes occupies this physically and chemically heterogeneous pore space. Although, in recent decades the consensus has largely been established, that microbial processes are strongly affected by the architecture of the soil pore space and the patchiness of the substrate distribution within it, still, the integration of pore network characteristics in models of microbial activity is scarce. We use an individual-based modelling approach to address the following questions:How does pore network architecture affect the efficiency of microbial organic matter decomposition? How do pore network properties like average node degree, shortest path length, and clustering coefficient affect the efficiency of organic matter decomposition? What is the effect of additional heterogeneity in pore sizes or distribution of substrate between pores on microbial efficiency? To incorporate the spatial structure the soil pore space that forms microhabitats is modelled as nodes of a network. Specific attributes are assigned to the nodes to describe their physical and biochemical conditions. Microbes inhabit a certain fraction of microhabitats (nodes) of the network and degrade organic matter that is available to them. Depending on microbial growth neighboring pores can be invaded  through the connecting links.  We were able to identify a number of network properties that affect the spread of microorganisms trough the network and the subsequent decomposition efficiency of the total substrate available in the system. While high clustering of nodes enables nearly complete decomposition of substrate, the presence of highly connected nodes (hubs) can decrease the efficiency of decomposition and lead to higher amount of substrate that remains undegraded. Regarding microbial growth parameters, the system shows a threshold behaviour. If microbial growth stays below a certain threshold value, microbes live only in the initially occupied pores and are not able to invade new pores. When the substrate concentration or the growth rate reaches the threshold value, there is a jump to large-scale invasion of all reachable pores in the network and much higher efficiency in the decomposition. In addition, high heterogeneity in substrate concentration or pore sizes lead to lower invasion efficiency, lower decomposition rate and a higher amount of substrate that is left at the end. Overall, we found that the spatial structure of the pore network had a more pronounced effect on microbial decomposition efficiencies than microbial physiological parameters, such as maximum microbial growth rates or extracellular enzyme kinetics.  Our findings allow for better understanding of the impact of soil pore network architecture on microbial processes. This is of high relevance when modelling the response of soil microbial communities to climate change.