Microscale Heterogeneity of the Spatial Distribution of Organic Matter Can Promote Bacterial Biodiversity in Soils: Insights From Computer Simulations

Abstract

There is still no satisfactory understanding of the factors that enable soil microbial populations to be as highly biodiverse as they are. The present article explores in silico the hypothesis that the heterogeneous distribution of soil organic matter, in addition to the spatial connectivity of the soil moisture, might account for the observed microbial biodiversity in soils. A multi-species, individual-based, pore-scale model is developed and parameterized with data from 3 Arthrobacter sp. strains, known to be, respectively, competitive, versatile, and poorly competitive. In the simulations, bacteria of each strain are distributed in a 3D computed tomography (CT) image of a real soil and three water saturation levels (100, 50, and 25%) and spatial heterogeneity levels (high, intermediate, and low) in the distribution of the soil organic matter are considered. High and intermediate heterogeneity levels assume, respectively, an amount of particulate organic matter (POM) distributed in a single (high heterogeneity) or in four (intermediate heterogeneity) randomly placed fragments. POM is hydrolyzed at a constant rate following a first-order kinetic, and continuously delivers dissolved organic carbon (DOC) into the liquid phase, where it is then taken up by bacteria. The low heterogeneity level assumes that the food source is available from the start as DOC. Unlike the relative abundances of the 3 strains, the total bacterial biomass and respiration are similar under the high and intermediate resource heterogeneity schemes. The key result of the simulations is that spatial heterogeneity in the distribution of organic matter influences the maintenance of bacterial biodiversity. The least competing strain, which does not reach noticeable growth for the low and intermediate spatial heterogeneities of resource distribution, can grow appreciably and even become more abundant than the other strains in the absence of direct competition, if the placement of the resource is favorable. For geodesic distances exceeding 5 mm, microbial colonies cannot grow. These conclusions are conditioned by assumptions made in the model, yet they suggest that microscale factors need to be considered to better understand the root causes of the high biodiversity of soils.

Spatial Control of Carbon Dynamics in Soil by Microbial Decomposer Communities

“…Strong spatial clustering of microbial communities, however, induces diffusionlimited C availability at the microhabitat scale which translates into lower decomposition of C compounds and microbial growth at the cm scale. This finding corroborates previous results indicating that the spatial separation of substrates and decomposers can be compensated to a certain degree by shifts in the functional composition of the microbial community (Kaiser et al, 2015), but that if critical diffusion lengths are reached, diffusive transport strongly controls C turnover at the microhabitat scale (Folse and Allison, 2012;Manzoni et al, 2014;Portell et al, 2018).…”

“…The simulated behavior of microbial functional groups supports experimental evidence of the importance of metabolic activation/deactivation strategies by microbial functional groups for regulating C turnover in soil (Placella et al, 2012;Joergensen and Wichern, 2018;Salazar et al, 2019). Our finding that interactions between microbial functional groups are controlled by the spatial localization of microorganisms is in agreement with previous results from individual-based modeling (Allison, 2005;Kaiser et al, 2015;Portell et al, 2018). SpatC model results, however, suggest a less severe impact of cheaters on microbial functioning and C turnover.…”

“…Experimental evidence further suggests that C turnover is strongly determined by pore characteristics (Kravchenko and Guber, 2017;Juyal et al, 2019) and microbial activity is highest in pores between 10 and 300 µm (Kravchenko et al, 2019). Thus, an improved description of microbial C turnover could be gained by integrating realistic descriptions of soil pore structure based on X-ray computed tomography data (see e.g., Portell et al, 2018) in combination with a meaningful correlation structure of substrate and microbial group distribution using evidence-based spatial statistical modeling. In addition, the representation of biological community interactions remains limited.…”

“…have indicated microscale (µm) control of bacterial diversity driven by the degree of heterogeneity in the spatial distribution of organic matter (Portell et al, 2018). In these simulations, the spatial heterogeneity of organic matter affected the succession of functional bacterial types differing in growth rates and substrate affinities.…”

Application of a Cellular Automaton Method to Model the Structure Formation in Soils Under Saturated Conditions: A Mechanistic Approach

“…While simulations on explicit pore structures of soils have become feasible in the last decade (e.g., Blunt et al, 2013) they do not account for an evolution of the rigid structures. Portell et al (2018), e.g., established an individual based model approach to account for growth of microbial species on explicit pore geometries, and combined it with solute transport realized by a Lattice Boltzmann method. The solid structure is fixed, however.…”