Browsing by Author "Baveye, Philippe C."
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Item Open Access Accounting for soil architecture and microbial dynamics in microscale models: current practices in soil science and the path ahead(Wiley, 2021-07-04) Pot, Valérie; Portell, Xavier; Otten, Wilfred; Garnier, Patricia; Monga, Olivier; Baveye, Philippe C.Macroscopic models of soil organic matter (SOM) turnover have faced difficulties in reproducing SOM dynamics or in predicting the spatial distribution of carbon stocks. These models are based on a largely inadequate linear response of soil microorganisms to bulk concentrations of nutrients and it is clear that a new approach to SOM modelling is required. Introducing explicit microbial activity and organic matter (OM) reactivity in macroscopic models represents a challenge because of the fine spatial scales at which the processes occur. To get a better grasp on interactions that take place at the microscale, a new generation of SOM models have been developed at the spatial scale of the soil microenvironments where microorganisms evolve. These models are well adapted to challenge traditional hypotheses about the influence of soil architecture on soil microbial activity. Soil architecture provides the stage for a dynamic spatial accessibility of resources to microbes and the emergence of interactions between the actors in SOM decomposition. In this context, we review microscale models of microbial activity that have been designed for soils and soil analogues. To understand how these models account for spatial accessibility, we look in detail at how soil microenvironments are described in the different approaches and how microbial colonies are spatialized in these microenvironments. We present the advantages and disadvantages of the developed strategies and we discuss their limits.Item Open Access Combination of techniques to quantify the distribution of bacteria in their soil microhabitats at different spatial scales(Elsevier, 2018-04-08) Juyal, Archana; Otten, Wilfred; Falconer, Ruth; Hapca, Simona; Schmidt, Hannes; Baveye, Philippe C.; Eickhorst, ThiloTo address a number of issues of great societal concern at the moment, like the sequestration of carbon, information is direly needed about interactions between soil architecture and microbial dynamics. Unfortunately, soils are extremely complex, heterogeneous systems comprising highly variable and dynamic micro-habitats that have significant impacts on the growth and activity of inhabiting microbiota. Data remain scarce on the influence of soil physical parameters characterizing the pore space on the distribution and diversity of bacteria. In this context, the objective of the research described in this article was to develop a method where X-ray microtomography, to characterize the soil architecture, is combined with fluorescence microscopy to visualize and quantify bacterial distributions in resin-impregnated soil sections. The influence of pore geometry (at a resolution of 13.4 μm) on the distribution of Pseudomonas fluorescens was analysed at macro- (5.2 mm × 5.2 mm), meso- (1 mm × 1 mm) and microscales (0.2 mm × 0.2 mm) based on an experimental setup simulating different soil architectures. The cell density of P. fluorescens was 5.59 x 107(SE 2.6 x 106) cells g−1 soil in 1–2 mm and 5.84 x 107(SE 2.4 x 106) cells g−1 in 2–4 mm size aggregates soil. Solid-pore interfaces influenced bacterial distribution at micro- and macroscale, whereas the effect of soil porosity on bacterial distribution varied according to three observation scales in different soil architectures. The influence of soil porosity on the distribution of bacteria in different soil architectures was observed mainly at the macroscale, relative to micro- and mesoscales. Experimental data suggest that the effect of pore geometry on the distribution of bacteria varied with the spatial scale, thus highlighting the need to consider an “appropriate spatial scale” to understand the factors that regulate the distribution of microbial communities in soils. The results obtained to date also indicate that the proposed method is a significant step towards a full mechanistic understanding of microbial dynamics in structured soils.Item Open Access Control of pore geometry in soil microcosms and its effect on the growth and spread of Pseudomonas and Bacillus sp.(Frontiers, 2018-07-13) Juyal, Archana; Eickhorst, Thilo; Falconer, Ruth; Baveye, Philippe C.; Spiers, Andrew; Otten, WilfredSimplified experimental systems, often referred to as microcosms, have played a central role in the development of modern ecological thinking on issues ranging from competitive exclusion to examination of spatial resources and competition mechanisms, with important model-driven insights to the field. It is widely recognized that soil architecture is the key driver of biological and physical processes underpinning ecosystem services, and the role of soil architecture and soil physical conditions is receiving growing interest. The difficulty to capture the architectural heterogeneity in microcosms means that we typically disrupt physical architecture when collecting soils. We then use surrogate measures of soil architecture such as aggregate size distribution and bulk-density, in an attempt to recreate conditions encountered in the field. These bulk-measures are too crude and do not describe the heterogeneity at microscopic scales where microorganisms operate. In the current paper we therefore ask the following questions: (i) To what extent can we control the pore geometry at microscopic scales in microcosm studies through manipulation of common variables such as density and aggregate size?; (ii) What is the effect of pore geometry on the growth and spread dynamics of bacteria following introduction into soil? To answer these questions, we focus on Pseudomonas sp. and Bacillus sp. We study the growth of populations introduced in replicated microcosms packed at densities ranging from 1.2 to 1.6 g cm−3, as well as packed with different aggregate sizes at identical bulk-density. We use X-ray CT and show how pore geometrical properties at microbial scales such as connectivity and solid-pore interface area, are affected by the way we prepare microcosms. At a bulk-density of 1.6 g cm−3 the average number of Pseudomonas was 63% lower than at a bulk-density of 1.3 g cm−3. For Bacillus this reduction was 66%. Depending on the physical conditions, bacteria in half the samples took between 1.62 and 9.22 days to spread 1.5 cm. Bacillus did spread faster than Pseudomonas and both did spread faster at a lower bulk-density. Our results highlight the importance that soil physical properties be considered in greater detail in soil microbiological studies than is currently the case.Item Open Access Emergent properties of microbial activity in heterogeneous soil microenvironments: different research approaches are slowly converging, yet major challenges remain(Frontiers Media, 2018-08-27) Baveye, Philippe C.; Otten, Wilfred; Kravchenko, Alexandra; Balseiro-Romero, María; Beckers, Éléonore; Chalhoub, Maha; Darnault, Christophe; Eickhorst, Thilo; Garnier, Patricia; Hapca, Simona; Kiranyaz, Serkan; Monga, Olivier; Mueller, Carsten W.; Nunan, Naoise; Pot, Valérie; Schlüter, Steffen; Schmidt, Hannes; Vogel, Hans-JörgOver 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.Item Open Access A holistic perspective on soil architecture is needed as a key to soil functions(Wiley, 2021-07-26) Vogel, Hans-Jörg; Balseiro-Romero, María; Kravchenko, Alexandra; Otten, Wilfred; Pot, Valérie; Schlüter, Steffen; Weller, Ulrich; Baveye, Philippe C.Soil functions, including climate regulation and the cycling of water and nutrients, are of central importance for a number of environmental issues of great societal concern. To understand and manage these functions, it is crucial to be able to quantify the structure of soils, now increasingly referred to as their “architecture”, as it constraints the physical, chemical, and biological processes in soils. This quantification was traditionally approached from two different angles, one focussed on aggregates of the solid phase, and the other on the pore space. The recent development of sophisticated, non-disturbing imaging techniques has led to significant progress in the description of soil architecture, in terms of both the pore space and the spatial configuration of mineral and organic materials. We now have direct access to virtually all aspects of soil architecture. In the present article, we review how this affects the perception of soil architecture specifically when trying to describe the functions of soils. A key conclusion of our analysis is that soil architecture, in that context, imperatively needs to be explored in its natural state, with as little disturbance as possible. The same requirement applies to the key processes taking place in the hierarchical soil pore network, including those contributing to the emergence of a heterogeneous organo-mineral soil matrix by various mixing processes such as bioturbation, diffusion, microbial metabolism and organo-mineral interactions. Artificially isolated aggregates are fundamentally inappropriate to derive conclusions about the functioning of an intact soil. To fully account for soil functions, we argue that a holistic approach that centres on the pore space is mandatory while the dismantlement of soils into chunks may still be carried out to study the binding of soil solid components. In the future, significant progress is expected along this holistic direction, as new, advanced technologies become available.Item Open Access Influence of soil structure on the spread of Pseudomonas fluorescens in soil at microscale(Wiley, 2020-04-24) Juyal, Archana; Otten, Wilfred; Baveye, Philippe C.; Eickhorst, ThiloFor over a half a century, researchers have been aware of the fact that the physical and chemical characteristics of microenvironments in soils strongly influence the activity, growth, and metabolism of microorganisms. However, many aspects of the effect of soil physical characteristics, such as the pore geometry, remain poorly understood. Therefore, the objective of the present research was to determine the influence of soil pore characteristics on the spread of bacteria, observed at the scale relevant to microbes. Pseudomonas fluorescens was introduced in columns filled with 1–2 mm soil aggregates, packed at different bulk densities.. Soil microcosms were scanned at 10.87 μm voxel resolution using X‐ray computed tomography (CT) to characterize the geometry of pores. Thin sections were prepared to determine the spread and colonization of bacteria. The results showed that average bacterial cell density was 174 cells mm−2 in soil with bulk density of 1.3 g cm−3 and 99 cells mm−2 in soil with bulk density of 1.5 g cm−3. Soil porosity and solid‐pore interfaces influence the spread of bacteria and their colonization of the pore space at lower bulk density, resulting in relatively higher bacterial densities in larger pore spaces. The study also demonstrates that thin sectioning of resin impregnated soil samples can be combined with X‐ray CT to visualize bacterial colonization of a 3D pore volume. This research therefore represents a significant step towards understanding how environmental change and soil management impact bacterial diversity in soils.Item Open Access Lessons from a landmark 1991 article on soil structure: distinct precedence of non-destructive assessment and benefits of fresh perspectives in soil research(CSIRO Publishing, 2022-01-19) Baveye, Philippe C.; Balseiro-Romero, María; Bottinelli, Nicolas; Briones, María; Capowiez, Yvan; Garnier, Patricia; Kravchenko, Alexandra; Otten, Wilfred; Pot, Valérie; Schlüter, Steffen; Vogel, Hans-JörgIn 1991, at the launch of a national symposium devoted to soil structure, the Australian Society of Soil Science invited Professor John Letey to deliver a keynote address, which was later published in the society’s journal. In his lecture, he shared the outcome of his reflexion about what the assessment of soil structure should amount to, in order to produce useful insight into the functioning of soils. His viewpoint was that the focus should be put on the openings present in the structure, rather than on the chunks of material resulting from its mechanical dismantlement. In the present article, we provide some historical background for Letey’s analysis, and try to explain why it took a number of years for the paradigm shift that he advocated to begin to occur. Over the last decade, his perspective that soil structure needs to be characterised via non-destructive methods appears to have gained significant momentum, which is likely to increase further in the near future, as we take advantage of recent technological advances. Other valuable lessons that one can derive from Letey’s pioneering article relate to the extreme value for everyone, even neophytes, to constantly ask questions about where research on given topics is heading, what its goals are, and whether the methods that are used at a certain time are optimal.Item Open Access Microscale heterogeneity of the spatial distribution of organic matter can promote bacterial biodiversity in soils: Insights from computer simulations(Frontiers Media, 2018-07-27) Portell, Xavier; Pot, Valérie; Garnier, Patricia; Otten, Wilfred; Baveye, Philippe C.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.Item Open Access Pore-scale monitoring of the effect of microarchitecture on fungal growth in a two-dimensional soil-like micromodel(Frontiers Media, 2018-07-03) Soufan, Raghad; Delaunay, Yolaine; Vieublé Gonod, Laure; Shor, Leslie M.; Garnier, Patricia; Otten, Wilfred; Baveye, Philippe C.In spite of the very significant role that fungi are called to play in agricultural production and climate change over the next two decades, very little is known at this point about the parameters that control the spread of fungal hyphae in the pore space of soils. Monitoring of this process in 3 dimensions is not technically feasible at the moment. The use of transparent micromodels simulating the internal geometry of real soils affords an opportunity to approach the problem in 2 dimensions, provided it is confirmed that fungi would actually want to propagate in such artificial systems. In this context, the key objectives of the research described in this article are to ascertain, first, that the fungus Rhizoctonia solani can indeed grow in a micromodel of a sandy loam soil, and, second, to identify and analyze in detail the pattern by which it spreads in the tortuous pores of the micromodel. Experimental observations show that hyphae penetrate easily inside the micromodel, where they bend frequently to adapt to the confinement to which they are subjected, and branch at irregular intervals, unlike in current computer models of the growth of hyphae, which tend to describe them as series of straight tubular segments. A portion of the time, hyphae in the micromodels also exhibit thigmotropism, i.e., tend to follow solid surfaces closely. Sub-apical branching, which in unconfined situations seems to be controlled by the fungus, appears to be closely connected with the bending of the hyphae, resulting from their interactions with surfaces. These different observations not only indicate different directions to follow to modify current mesoscopic models of fungal growth, so they can apply to soils, but they also suggest a wealth of further experiments using the same set-up, involving for example competing fungal hyphae, or the coexistence of fungi and bacteria in the same pore space.Item Open Access Scenario modelling of carbon mineralization in 3D soil architecture at the microscale: toward an accessibility coefficient of organic matter for bacteria(Wiley, 2021-07-07) Mbé, Bruno; Monga, Olivier; Pot, Valérie; Otten, Wilfred; Hecht, Frédéric; Raynaud, Xavier; Nunan, Naoise; Chenu, Claire; Baveye, Philippe C.; Garnier, PatriciaThe microscale physical characteristics of microbial habitats considerably affect the decomposition of organic matter in soils. One of the challenges is to identify microheterogeneities in soil that can explain the extent of carbon mineralization. The aim of this study was therefore to identify descriptors of μm-scale soil heterogeneity that can explain CO2 fluxes obtained at the mm scale. A suite of methods and models that visualize soil heterogeneity at scales relevant to microorganisms has been developed over the last decade. Among the existing 3D models that simulate microbial activity in soils, Mosaic is able to simulate, within a short computation time, the microbial degradation of organic matter at the microhabitat scale in soil using real 3D images of soil porosity. Our approach was to generate scenarios of carbon mineralization for various microscale environmental conditions and determine how the descriptors of soil structure could explain CO2 evolution. First, we verified that the simulated diffusion of solutes in the soil samples obtained with Mosaic were the same as those obtained using the same parameter set from a robust 3D model based on a lattice Boltzmann approach. Then, we ran scenarios considering different soil pore architectures, water saturations and microorganism and organic matter placements. We found that the CO2 emissions simulated for the different scenarios could be explained by the distance between microorganisms and organic matter, the diffusion of the substrate and the concentration of the available substrate. For some of the scenarios, we proposed a descriptor of accessibility based on the geodesic distance between microorganisms and organic matter weighted by the amount of organic matter. This microscale descriptor is correlated to the simulated CO2 flux with a correlation coefficient of 0.69.Item Open Access ‘Shifting gears ain't easy’: Disciplinary resistances to perspective shifts in soil science and how to move forward(Wiley, 2024-11-01) Baveye, Philippe C.; Otten, Wilfred; Young, IainOver the last decade, the fact that novel perspectives on various aspects of soils have remained strongly controversial long after they emerged, without any kind of consensus being reached about them, raises question about the underlying reasons for this phenomenon. The on‐going debate on the usefulness of aggregates to describe the functions of soils illustrates some of the key aspects of that question. Similar debates on other soil‐related issues also appear stalled, or have been for a long time and are only now moving forward. This might suggest a fundamental aversion to change, which when it gets overcome, only does so slowly. However, at the same time, somewhat surprisingly, researchers appear willing to quickly seize opportunities provided by new idea or novel perspectives on other topics. In that context, the objective of the present article is to analyse in detail what may cause such contrasting reactions to novelty. We consider, then ultimately dismiss, explanations based on how strongly or not novel perspectives have been actively promoted, on how access to suitable technology may impede or only slow down perspective shifts and on whether a recent theory of the ‘slowed canonical progress in large fields of science’ applies to the relatively small soil science community. Then, taking soil aggregates as a case in point, we come to realize that it is the extent to which a novel perspective mandates an interdisciplinary approach that determines whether or not it is adopted quickly. From that standpoint, we envisage a number of practical actions that could be taken to facilitate in the future the emergence in soil science of interdisciplinary research efforts, which we argue are absolutely essential to successfully tackle the enormous complexity of soils and to come up with satisfactory answers to the daunting environmental and food security problems we currently face in their management.Item Open Access Soil aggregates as biogeochemical reactors: Not a way forward in the research on soil‐atmosphere exchange of greenhouse gases(Wiley, 2019-04-08) Kravchenko, Alexandra; Otten, Wilfred; Garnier, Patricia; Pot, Valérie; Baveye, Philippe C.Over the last two decades, the fact that soils are significant sources of greenhouse gases (GHG), e.g., carbon dioxide (CO2), methane (CH4), nitrous oxide (N2O), and water vapor, has received considerable attention from the scientific community. Many laboratory and field experiments have been carried out to investigate the release of GHG by soils, and a wide range of computer modeling approaches have been explored to encapsulate what is known about the process, as well as to improve its prediction at various spatial and temporal scales.Item Open Access Understanding the joint impacts of soil architecture and microbial dynamics on soil functions: insights derived from microscale models(Wiley, 2022-06-23) Pot, Valérie; Portell, Xavier; Otten, Wilfred; Garnier, Patricia; Monga, Olivier; Baveye, Philippe C.Over the last decades, a new generation of microscale models has been developed to simulate soil microbial activity. An earlier article (Pot et al., 2021) presented a detailed review of the description of soil architecture and microbial dynamics in these models. In the present article, we summarise the main results obtained by these models according to six model outputs: growth and spatial organisation of microbial colonies, soil hydraulic conductivity, coexistence and trophic interactions of microorganisms, temporal dynamics of the amount of solid and dissolved organic matter in soil and, microbial production of CO2. For each of these outputs, we draw particular attention to the respective roles of soil architecture and microbial dynamics, and we report how microscale models allow for disentangling and quantifying them. We finally discuss limitations and future directions of microscale models in combination with the on-going development of high-performance imaging tools revealing the spatial heterogeneity of the actors of soil microbial activity.