Opportunities and limits in imaging microorganisms and their activities in soil microhabitats

Védère, Charlotte; Laure, Vieublé Gonod; Nunan, Naoise; Chenu, Claire

doi:10.1016/j.soilbio.2022.108807

Cited by 24 publications

(11 citation statements)

References 238 publications

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“…Second, interference of one imaging technique with another, e.g., by sputtering or material ablation via laser shots, should be minimized. 30 Based on the prerequisites of individual imaging techniques (Table 1) in the current study, this resulted in the following sequence: X-ray CT, light microscopy, μXRF, SEM, NanoSIMS, and LA-IRMS (Figure 1). The thinner the soil section, the more reflection from the sample holder was visible in the epifluorescence images (images not shown).…”

Section: Sequence Ofmentioning

confidence: 99%

“…The mentioned spectromicroscopic techniques often have common prerequisites for sample preparation as samples need to be dehydrated and vacuum stable. 30 Likewise, complex samples as for instance intact soil cores are oftentimes embedded and sectioned in a resin or agar matrix to preserve the structural integrity but the structural integrity before and after embedding is rarely checked. 23 Moreover, the unintentional modification of chemical gradients by colloid redistribution or solute leaching during sample preparation remains unclear.…”

Section: Introductionmentioning

confidence: 99%

“…23 Moreover, the unintentional modification of chemical gradients by colloid redistribution or solute leaching during sample preparation remains unclear. 30 The aim of the current study was to capture radial chemical gradients in the rhizosphere of well-characterized 3D root segments as a result of interacting processes at the interface between roots, microorganisms, and the soil matrix. To do so, we established a procedure for correlative image analysis of resin-embedded rhizosphere soil containing root types of a specific age.…”

Section: Introductionmentioning

confidence: 99%

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Correlative Imaging of the Rhizosphere─A Multimethod Workflow for Targeted Mapping of Chemical Gradients

Lippold

Schlüter

Mueller

et al. 2023

Environ. Sci. Technol.

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Examining in situ processes in the soil rhizosphere requires spatial information on physical and chemical properties under undisturbed conditions. We developed a correlative imaging workflow for targeted sampling of roots in their three-dimensional (3D) context and assessed the imprint of roots on chemical properties of the root–soil contact zone at micrometer to millimeter scale. Maize (Zea mays) was grown in 15N-labeled soil columns and pulse-labeled with 13CO2 to visualize the spatial distribution of carbon inputs and nitrogen uptake together with the redistribution of other elements. Soil columns were scanned by X-ray computed tomography (X-ray CT) at low resolution (45 μm) to enable image-guided subsampling of specific root segments. Resin-embedded subsamples were then analyzed by X-ray CT at high resolution (10 μm) for their 3D structure and chemical gradients around roots using micro-X-ray fluorescence spectroscopy (μXRF), nanoscale secondary ion mass spectrometry (NanoSIMS), and laser-ablation isotope ratio mass spectrometry (LA-IRMS). Concentration gradients, particularly of calcium and sulfur, with different spatial extents could be identified by μXRF. NanoSIMS and LA-IRMS detected the release of 13C into soil up to a distance of 100 μm from the root surface, whereas 15N accumulated preferentially in the root cells. We conclude that combining targeted sampling of the soil–root system and correlative microscopy opens new avenues for unraveling rhizosphere processes in situ.

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Section: Sequence Ofmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Correlative Imaging of the Rhizosphere─A Multimethod Workflow for Targeted Mapping of Chemical Gradients

Lippold

Schlüter

Mueller

et al. 2023

Environ. Sci. Technol.

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“…global) (Levins, 1966;Livingtson, 1985). Additionally, the increasing recognition of soil habitat structure for organic matter storage and stability (Cotrufo et al, 2013;Kravchenko et al, 2019a;King, 2020), as well as for community assembly and biodiversity maintenance (Erktan et al, 2017;Charlotte et al, 2022;Schweizer, 2022;Vogel et al, 2022), highlights the potential utility of re-conceptualizing how the soil environment is modeled and formulated. Given the breadth of services that soils offer, adopting modeling strategies that are transferable across soil ecology sub-disciplines (Buchkowski et al, 2017) indeed helps move toward addressing the most general of goals in soil ecology, such as how soil biotic and abiotic spheres or networks interact over time to confer bulk soil properties.…”

Section: Introductionmentioning

confidence: 99%

Developing systems theory in soil agroecology: Incorporating heterogeneity and dynamic instability

Medina¹,

Vandermeer²

2023

Preprint

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Ecosystem management is integral to the future of soils, yet anthropogenic drivers represent a key source of uncertainty in ecosystem models. First- and new-generation soil models formulate many soil pools using first-order decomposition, which tends to generate simpler yet numerous parameters. Systems or complexity theory, developed across various scientific and social fields, may help improve robustness of soil models, by offering consistent assumptions about system openness, potential dynamic instability and distance from commonly assumed stable equilibria, as well as new analytical tools for formulating more generalized model structures that reduce parameter space and yield a wider array of possible model outcomes, such as quickly shrinking carbon stocks with pulsing or lagged respiration. This paper builds on recent perspectives of soil modeling to ask how various soil functions can be better understood by applying a complex systems lens. We synthesized previous literature reviews with concepts from non-linear dynamical systems in theoretical ecology and soil sciences more broadly to identify areas for further study that may help improve the robustness of soil models under the uncertainty of human activities and management. Three broad dynamical concepts were highlighted: soil variable memory or state-dependence, oscillations, and tipping points or hysteresis. These themes represent less intuitive yet key dynamics that can emerge after assuming nuanced observations, such as reversibility of organo-mineral associations, dynamic aggregate- and pore hierarchies, persistent wet-dry cycles, higher-order microbial community and predator-prey interactions, cumulative legacy land use history, and social management interactions and/or cooperation. We discuss how these aspects may contribute useful analytical tools, metrics, and frameworks that help integrate the uncertainties in future soil states, ranging from micro- to regional scales, including those indirectly affected by human activities and management decisions. Overall, this study highlights the potential benefits of incorporating spatial heterogeneity and dynamic instabilities into future model representations of whole soil processes. Additionally, it advocates for transdisciplinary collaborations between natural and social scientists, extending research into anthropedology and biogeosociochemistry, to better integrate and understand longer-term anthropogenic drivers of soil processes, potentially from soil structural dynamics to microbial community and food web ecology.

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“…Invertebrate soil ecosystem engineers are widely recognized for their fundamental roles in shaping ecosystems (Perfecto, Vandermeer, and Philpott 2014), soil habitats (Jouquet et al 2006; Lavelle et al 2016), biodiversity (Thakur et al 2020; Lavelle et al 2022), and related processes (McGlynn and Poirson 2012; Filser et al 2016), although they are less studied compared to soil microbes (van der Heijden, Bardgett, and van Straalen 2008; Banerjee and van der Heijden 2022; Charlotte et al 2022). Extended phenotype engineers (Jouquet et al 2006), namely ants, have been shown to affect soil geomorphology (Whitford and Eldridge 2013) including: changes in texture and lower bulk density (Dostál et al 2005; Cammeraat and Risch 2008); an increase in general microporosity (Tschinkel 2005), water infiltration (Cerdà, Jurgensen, and Bodi 2009) and water availability (X. R. Li et al 2014); increased soil nutrient availability (Wagner, Brown, and Gordon 1997; Wagner, Jones, and Gordon 2004; Shukla et al 2013; Kotova, Umarov, and Zakalyukina 2015; Sankovitz and Purcell 2022) but lower availability of metals (Gramigni et al 2013); increased plant root and shoot growth (Farji-Brener and Werenkraut 2017); and recently, also increase microbial diversity (Delgado-baquerizo et al 2019; Baker et al 2020) and changed community structure, including even by non-fungal specialist ants (Lindström et al 2019), in addition to fungal specialist (i.e.…”

Section: Introductionmentioning

confidence: 99%

Above- and below-ground links mediated by arboreal ants and host tree modify soil aggregation scaling, infiltration, and chemistry

Medina,

Schmitt,

Perfecto

et al. 2023

Preprint

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Soils are increasingly recognized as complex systems, emphasizing a need to study unique properties such as long-tailed scaling laws and the role of indirect interactions among arboreal above- and below-ground soil invertebrates. However, few studies consider the above-below-ground connections mediated by invertebrates’ activity and behavior compared to mediated by tree physiology. Given previous work showing that arboreal ants can compete and affect ground foragers as well as alter foraging behavior on different host trees, it is plausible that persistent above-ground ant nesting could extend to affect soil properties including structure and chemistry, mediated by ground ant exclusion. This study analyzes soil aggregation, water infiltration, and macro-chemical data associated with longer-term (5+ year) ant nesting in a rustic tropical agroforest. Results show that, 1) ant nesting maintained scaling law exponents or fractal dimensions of soil aggregate size distributions, and was significantly associated with relatively larger micro-aggregate diameters and log-normal variance in macro-aggregate size distributions, suggesting more consistent (less variable) underlying aggregation processes similar to host tree species effects; 2) areas in the vicinity of trees with no dominant ant nests had three-times faster water infiltration than in the vicinity of trees with dominant ant nests; and 3) a tendency toward changes in soil carbon and nitrogen stocks by one-quarter depending on host tree. These patterns are consistent with expected effects of ground ant suppression by an aggressive keystone arboreal ant, and are supported by previous studies reporting positive ground ant nest effects on soil chemistry and documenting ground ant foraging as a source of soil aggregate fragmentation. This study presents new ecological processes affecting ecosystem-scale functions, and suggests that future research on indirect interaction cascades would be beneficial to advance fundamental understanding of whole-ecosystem processes.

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Opportunities and limits in imaging microorganisms and their activities in soil microhabitats

Cited by 24 publications

References 238 publications

Correlative Imaging of the Rhizosphere─A Multimethod Workflow for Targeted Mapping of Chemical Gradients

Correlative Imaging of the Rhizosphere─A Multimethod Workflow for Targeted Mapping of Chemical Gradients

Developing systems theory in soil agroecology: Incorporating heterogeneity and dynamic instability

Above- and below-ground links mediated by arboreal ants and host tree modify soil aggregation scaling, infiltration, and chemistry

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