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Front Microbiol. 2018 Aug 27;9:1929. doi: 10.3389/fmicb.2018.01929. eCollection 2018.

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

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UMR ECOSYS, AgroParisTech, Université Paris-Saclay, Thiverval-Grignon, rance.
School of Water, Energy and Environment, Cranfield University, Cranfield, United Kingdom.
Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI, United States.
Department of Soil Science and Agricultural Chemistry, Centre for Research in Environmental Technologies, Universidade de Santiago de Compostela, Santiago de Compostela, Spain.
Soil-Water-Plant Exchanges, Terra Research Centre, BIOSE, Gembloux Agro-Bio Tech, University of Liège, Gembloux, Belgium.
UMR ECOSYS, INRA, Université Paris-Saclay, Thiverval-Grignon, France.
Laboratory of Hydrogeoscience and Biological Engineering, L.G. Rich Environmental Laboratory, Department of Environmental Engineering and Earth Sciences, Clemson University, Clemson, SC, United States.
Faculty 2 Biology/Chemistry, University of Bremen, Bremen, Germany.
Dundee Epidemiology and Biostatistics Unit, School of Medicine, University of Dundee, Dundee, United Kingdom.
Department of Electrical Engineering, Qatar University, Doha, Qatar.
Institut de Recherche pour le Développement, Bondy, France.
Lehrstuhl für Bodenkunde, Technical University of Munich, Freising, Germany.
Institute of Ecology and Environmental Sciences - Paris, Sorbonne Universités, CNRS, IRD, INRA, P7, UPEC, Paris, France.
Soil System Science, Helmholtz-Zentrum für Umweltforschung GmbH - UFZ, Leipzig, Germany.
Terrestrial Ecosystem Research, Department of Microbiology and Ecosystem Science, Research Network 'Chemistry meets Microbiology', University of Vienna, Vienna, Austria.
Institute of Soil Science and Plant Nutrition, Martin Luther University of Halle-Wittenberg, Halle, Germany.


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.


NanoSIMS imaging; X-ray computed; biodiversity; single-cell genomics; soil microbiology; tomography; upscaling

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