Emergent Properties of Microbial Activity in Heterogeneous Soil Microenvironments: Different Research Approaches Are Slowly Converging, Yet Major Challenges Remain

Abstract

Over the last 60 years, soil microbiologists have accumulated a wealth of experimental data showing that the bulk, macroscopic parameters (e.g., granulometry, pH, soil organic matter, and biomass contents) commonly used to characterize soils provide insufficient information to describe quantitatively the activity of soil microorganisms and some of its outcomes, like the emission of greenhouse gasses. Clearly, new, more appropriate macroscopic parameters are needed, which reflect better the spatial heterogeneity of soils at the microscale (i.e., the pore scale) that is commensurate with the habitat of many microorganisms. For a long time, spectroscopic and microscopic tools were lacking to quantify processes at that scale, but major technological advances over the last 15 years have made suitable equipment available to researchers. In this context, the objective of the present article is to review progress achieved to date in the significant research program that has ensued. This program can be rationalized as a sequence of steps, namely the quantification and modeling of the physical-, (bio)chemical-, and microbiological properties of soils, the integration of these different perspectives into a unified theory, its upscaling to the macroscopic scale, and, eventually, the development of new approaches to measure macroscopic soil characteristics. At this stage, significant progress has been achieved on the physical front, and to a lesser extent on the (bio)chemical one as well, both in terms of experiments and modeling. With regard to the microbial aspects, although a lot of work has been devoted to the modeling of bacterial and fungal activity in soils at the pore scale, the appropriateness of model assumptions cannot be readily assessed because of the scarcity of relevant experimental data. For significant progress to be made, it is crucial to make sure that research on the microbial components of soil systems does not keep lagging behind the work on the physical and (bio)chemical characteristics. Concerning the subsequent steps in the program, very little integration of the various disciplinary perspectives has occurred so far, and, as a result, researchers have not yet been able to tackle the scaling up to the macroscopic level. Many challenges, some of them daunting, remain on the path ahead. Fortunately, a number of these challenges may be resolved by brand new measuring equipment that will become commercially available in the very near future.

Disturbance Size Can Be Compensated for by Spatial Fragmentation in Soil Microbial Ecosystems

“…To further understand the roles of the explicit environmental structure and the disturbance type for functional resilience of microbial ecosystems, more experimental studies are needed. One promising approach to evaluate structural effects in microbial systems is the use of microfluidics or micromodels, especially in combination with the increasing resolution of imaging techniques (Connell et al, 2013;Aleklett et al, 2018;Baveye et al, 2018;Toju et al, 2018). They allow for the observation of microbial dynamics in different spatially structured setups mimicking various soil pore structures, and also the application of disturbances like drought or heat events.…”

Developments in Agricultural Soil Quality and Health: Reflections by the Research Committee on Soil Organic Matter Management

“…A pore-oriented approach that explores how soil biology interacts with surfaces to structure the soil and influences processes is likely to be more fruitful (Kravchenko and Guber, 2017;Rabot et al, 2018). Investment in newer methods (e.g., CT scanners) (Baveye et al, 2018) that quantify features regulating processes of interest might help us identify indicators that will be more predictive of soil services.…”

Spatial Control of Carbon Dynamics in Soil by Microbial Decomposer Communities

“…Yet, understanding how microbial community characteristics affect rates of biogeochemical processes remains a major research challenge. Further progress to quantitatively describe spatial arrangements between microorganisms in their micro-environment and their corresponding substrate is needed (Graham et al, 2016;Baveye et al, 2018).…”