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

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          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.

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          Most cited references582

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          The diversity and biogeography of soil bacterial communities.

          For centuries, biologists have studied patterns of plant and animal diversity at continental scales. Until recently, similar studies were impossible for microorganisms, arguably the most diverse and abundant group of organisms on Earth. Here, we present a continental-scale description of soil bacterial communities and the environmental factors influencing their biodiversity. We collected 98 soil samples from across North and South America and used a ribosomal DNA-fingerprinting method to compare bacterial community composition and diversity quantitatively across sites. Bacterial diversity was unrelated to site temperature, latitude, and other variables that typically predict plant and animal diversity, and community composition was largely independent of geographic distance. The diversity and richness of soil bacterial communities differed by ecosystem type, and these differences could largely be explained by soil pH (r(2) = 0.70 and r(2) = 0.58, respectively; P < 0.0001 in both cases). Bacterial diversity was highest in neutral soils and lower in acidic soils, with soils from the Peruvian Amazon the most acidic and least diverse in our study. Our results suggest that microbial biogeography is controlled primarily by edaphic variables and differs fundamentally from the biogeography of "macro" organisms.
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            Plant Growth-Promoting Bacteria: Mechanisms and Applications

            The worldwide increases in both environmental damage and human population pressure have the unfortunate consequence that global food production may soon become insufficient to feed all of the world's people. It is therefore essential that agricultural productivity be significantly increased within the next few decades. To this end, agricultural practice is moving toward a more sustainable and environmentally friendly approach. This includes both the increasing use of transgenic plants and plant growth-promoting bacteria as a part of mainstream agricultural practice. Here, a number of the mechanisms utilized by plant growth-promoting bacteria are discussed and considered. It is envisioned that in the not too distant future, plant growth-promoting bacteria (PGPB) will begin to replace the use of chemicals in agriculture, horticulture, silviculture, and environmental cleanup strategies. While there may not be one simple strategy that can effectively promote the growth of all plants under all conditions, some of the strategies that are discussed already show great promise.
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              Stability of organic carbon in deep soil layers controlled by fresh carbon supply.

              The world's soils store more carbon than is present in biomass and in the atmosphere. Little is known, however, about the factors controlling the stability of soil organic carbon stocks and the response of the soil carbon pool to climate change remains uncertain. We investigated the stability of carbon in deep soil layers in one soil profile by combining physical and chemical characterization of organic carbon, soil incubations and radiocarbon dating. Here we show that the supply of fresh plant-derived carbon to the subsoil (0.6-0.8 m depth) stimulated the microbial mineralization of 2,567 +/- 226-year-old carbon. Our results support the previously suggested idea that in the absence of fresh organic carbon, an essential source of energy for soil microbes, the stability of organic carbon in deep soil layers is maintained. We propose that a lack of supply of fresh carbon may prevent the decomposition of the organic carbon pool in deep soil layers in response to future changes in temperature. Any change in land use and agricultural practice that increases the distribution of fresh carbon along the soil profile could however stimulate the loss of ancient buried carbon.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                27 August 2018
                2018
                : 9
                : 1929
                Affiliations
                [1] 1UMR ECOSYS, AgroParisTech, Université Paris-Saclay , Thiverval-Grignon, rance
                [2] 2School of Water, Energy and Environment, Cranfield University , Cranfield, United Kingdom
                [3] 3Department of Plant, Soil and Microbial Sciences, Michigan State University , East Lansing, MI, United States
                [4] 4Department of Soil Science and Agricultural Chemistry, Centre for Research in Environmental Technologies, Universidade de Santiago de Compostela , Santiago de Compostela, Spain
                [5] 5Soil–Water–Plant Exchanges, Terra Research Centre, BIOSE, Gembloux Agro-Bio Tech, University of Liège , Gembloux, Belgium
                [6] 6UMR ECOSYS, INRA, Université Paris-Saclay , Thiverval-Grignon, France
                [7] 7Laboratory of Hydrogeoscience and Biological Engineering, L.G. Rich Environmental Laboratory, Department of Environmental Engineering and Earth Sciences, Clemson University , Clemson, SC, United States
                [8] 8Faculty 2 Biology/Chemistry, University of Bremen , Bremen, Germany
                [9] 9Dundee Epidemiology and Biostatistics Unit, School of Medicine, University of Dundee , Dundee, United Kingdom
                [10] 10Department of Electrical Engineering, Qatar University , Doha, Qatar
                [11] 11Institut de Recherche pour le Développement , Bondy, France
                [12] 12Lehrstuhl für Bodenkunde, Technical University of Munich , Freising, Germany
                [13] 13Institute of Ecology and Environmental Sciences – Paris, Sorbonne Universités, CNRS, IRD, INRA, P7, UPEC , Paris, France
                [14] 14Soil System Science, Helmholtz-Zentrum für Umweltforschung GmbH – UFZ , Leipzig, Germany
                [15] 15Terrestrial Ecosystem Research, Department of Microbiology and Ecosystem Science, Research Network ‘Chemistry meets Microbiology’, University of Vienna , Vienna, Austria
                [16] 16Institute of Soil Science and Plant Nutrition, Martin Luther University of Halle-Wittenberg , Halle, Germany
                Author notes

                Edited by: Eoin L. Brodie, Lawrence Berkeley National Laboratory (LBNL), United States

                Reviewed by: James J. Moran, Pacific Northwest National Laboratory (DOE), United States; Peter Nico, Lawrence Berkeley National Laboratory (LBNL), United States

                *Correspondence: Philippe C. Baveye, baveye.rpi@ 123456gmail.com

                This article was submitted to Terrestrial Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2018.01929
                6119716
                30210462
                7e236e3e-1452-4841-b410-c05426fdd5a2
                Copyright © 2018 Baveye, Otten, Kravchenko, Balseiro-Romero, Beckers, Chalhoub, Darnault, Eickhorst, Garnier, Hapca, Kiranyaz, Monga, Mueller, Nunan, Pot, Schlüter, Schmidt and Vogel.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 March 2018
                : 30 July 2018
                Page count
                Figures: 9, Tables: 0, Equations: 0, References: 616, Pages: 48, Words: 0
                Funding
                Funded by: Qatar National Research Fund 10.13039/100008982
                Award ID: NPRP grant #9-390-1-088
                Funded by: Agence Nationale de la Recherche 10.13039/501100000270
                Award ID: Projet Soilµ3D
                Funded by: Consellería de Cultura, Educación e Ordenación Universitaria, Xunta de Galicia 10.13039/501100008425
                Award ID: Programa de axudas á etapa posdoutoral;Â Â ED481B 2017/073
                Funded by: Natural Environment Research Council 10.13039/501100000270
                Award ID: NE/P014208/1
                Categories
                Microbiology
                Review

                Microbiology & Virology
                soil microbiology,biodiversity,upscaling,tomography,x-ray computed,nanosims imaging,single-cell genomics

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