Multi-lab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass

Sasse, Joëlle; Kant, Josefine; Cole, Benjamin; Klein, Andrew P.; Arsova, Borjana; Schlaepfer, Pascal; Lewald, Kyle M; Zhalnina, Kateryna; Kosina, Suzanne M.; Bowen, Benjamin P.; Treen, Daniel; Vogel, John P.; Visel, Axel; Watt, Michelle; Dangl, Jefferey L; Northen, Trent

doi:10.1101/435818

Cited by 11 publications

(17 citation statements)

References 53 publications

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“…In this study, exudates were collected from roots with rhizosphere substrate still attached. The largest difference in this dataset was observed between soil-grown and sand- or clay-grown plants, which might be explained by soil-derived metabolites co-extracted with root exudates (Sasse et al, 2018; Miller et al, 2019). The authors showed some ions to be specifically up- or down-regulated in exudates of clay- vs. sand-grown plants, but their effect was not strong enough to separate the two conditions in a principal component analysis (Miller et al, 2019), which might be due to their exudate collection method, which was a mixture between the in situ and in vitro conditions utilized here.…”

Section: Discussionmentioning

confidence: 94%

“…Thus, changes in root morphology of plants grown in phosphate-limited clay might be distinct from plants grown in phosphate-limited sand or glass beads. Plants grown in soil may exhibit additional changes in root morphology and metabolism, as shown for B. distachyon grown in a sterile soil extract, which showed reduced root length, elongated root hairs, and depleted a variety of metabolites from soil extract (Sasse et al, 2018). Root systems further respond to local alterations in soil structure, such as to the presence of micro- or macropores, or to air pockets (Rellán-Álvarez et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…We found that diffusion rates were limited in smaller particle sizes. In systems with low diffusion rates, exudate concentration is likely higher around the roots, which might lead to higher exudate re-uptake than in systems with larger particle sizes (Sherson et al, 2000; Sasse et al, 2018). It might thus be interesting to investigate if clays with different particle sizes might provoke a root morphology and exudation profile distinct from glass bead-grown plants.…”

Section: Discussionmentioning

confidence: 99%

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Root morphology and exudate availability is shaped by particle size and chemistry in Brachypodium distachyon

Sasse

Jordan

Raad

et al. 2019

Preprint

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Keywords Brachypodium distachyonParticle chemistry Particle size Pseudomonas fluorescens Rhizosphere Root exudation Root morphology Abstract Root morphology and exudation define a plants sphere of influence in soils, and are in turn shaped by the physiochemical characteristics of soil. We explored how particle size and chemistry of growth substrates affect root morphology and exudation of the model grass Brachypodium distachyon. Root fresh weight and root lengths were correlated with particle size, whereas root number and shoot weight remained constant. Mass spectrometry imaging suggested that both, root length and number shape root exudation. Exudate metabolite profiles detected with liquid chromatography / mass spectrometry were comparable for plants growing in glass beads or sand with various particles sizes, but distinct for plants growing in clay. However, when exudates of clay-grown plants were collected by removing the plants from the substrate, their exudate profile was similar to sand-or glass beads-grown plants. Clay particles sorbed 20% of compounds exuded by clay-grown plants, and 70% of compounds of a defined exudate medium. The sorbed compounds belonged to a range of chemical classes, among them nucleosides/nucleotides, organic acids, sugars, and amino acids. Some of the sorbed compounds could be de-sorbed by a rhizobacterium (Pseudomonas fluorescens WCS415), supporting its growth. We show that root morphology is affected by substrate size, and that root exudation in contrast is not affected by substrate size or chemistry. The availability of exuded compounds, however, depends on the substrate present. These findings further support the critical importance of the physiochemical properties of soils are crucial to consider when investigating plant morphology, exudation, and plantmicrobe interactions. Plant roots shape their environment in various ways, and are in turn shaped by physiochemical properties of the surrounding soil. Roots shape soil by dislocating particles, by polymer production, and by release of a wide variety of compounds (root exudation). Root exudates alter pH and the chemical composition around roots. Overall, root presence in soils results in formation of larger soil aggregates and increases water-holding capacity (Six et al., 2004). The plant-induced changes in chemistry can lead to weathering of minerals (Uroz et al., 2015), and alter the composition of microbial communities (Carson et al., 2007).Soils are often characterized by their particle size and mineralogy. Typical soil particles range from small (< 50 µm) to large (> 2 mm), determining physical parameters such as water binding capacity (Six et al., 2004; Six and Paustian, 2014; Rellán-Álvarez et al., 2016). Differently sized sandstones are associated with different microbial numbers, with small sandstones (2 mm) being more densely populated by microbes than larger rocks (Certini et al., 2004). Minerals differ in their structure (e.g. accessible surface), and in their surface charge, determining if and how they interact wi...

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Section: Discussionmentioning

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Root morphology and exudate availability is shaped by particle size and chemistry in Brachypodium distachyon

Sasse

Jordan

Raad

et al. 2019

Preprint

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“…Loss of nutrient ions with efflux water would be undesirable. It is possible nutrients may be specifically resorbed by the root with other exuded metabolites (see Sasse et al, 2019).…”

Section: Figmentioning

confidence: 99%

Dynamics in plant roots and shoots minimize stress, save energy and maintain water and nutrient uptake

et al. 2019

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Plants are inherently dynamic. Dynamics minimize stress while enabling plants to flexibly acquire resources. Three examples are presented for plants tolerating saline soil: transport of sodium chloride (NaCl), water and macronutrients is nonuniform along a branched root; water and NaCl redistribute between shoot and soil at night-time; and ATP for salt exclusion is much lower in thinner branch roots than main roots, quantified using a biophysical model and geometry from anatomy. Noninvasive phenotyping and precision agriculture technologies can be used together to harness plant dynamics, but analytical methods are needed. A plant advancing in time through a soil and atmosphere space is proposed as a framework for dynamic data and their relationship to crop improvement.

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“…This approach uses sigmoidal model fits to define the midpoint of substrate depletion from the media (t 50 ) and parse out substrate preferences during microbial growth. It has on October 31, 2020 by guest http://aem.asm.org/ Downloaded from been used in conjunction with both natural (37)(38)(39) and defined, complex medias (40) and shown the ability to link isolate exometabolite profiling with in situ community function (41).…”

Section: Introductionmentioning

confidence: 99%

Ecophysiological Study ofParaburkholderiasp. Strain 1N under Soil Solution Conditions: Dynamic Substrate Preferences and Characterization of Carbon Use Efficiency

Cyle

Klein

Aristilde

et al. 2020

Appl Environ Microbiol

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We used time-resolved metabolic footprinting, an important technical approach used to monitor changes in extracellular compound concentrations during microbial growth, to study the order of substrate utilization (i.e., substrate preferences) and kinetics of a fast-growing soil isolate, Paraburkholderia sp. 1N. The growth of Paraburkholderia sp. 1N was monitored under aerobic conditions in a soil-extracted, solubilized organic matter media, representing a realistic diversity of available substrates and gradient of initial concentrations. We combined multiple analytical approaches to track over 150 compounds in the media and complemented this with bulk carbon and nitrogen measurements, allowing estimates of carbon use efficiency throughout the growth curve. Targeted methods allowed the quantification of common low-molecular-weight substrates: glucose, 20 amino acids, and 9 organic acids. All targeted compounds were depleted from the media and depletion followed a sigmoidal curve where sufficient data were available. Substrates were utilized in at least three distinct temporal clusters as Paraburkholderia sp. 1N produced biomass at a cumulative carbon use efficiency of 0.43. The two substrates with highest initial concentrations, glucose and valine, exhibited longer usage windows, at higher biomass-normalized rates, and later in the growth curve. Contrary to hypotheses based on previous studies, we found no clear relationship between substrate nominal oxidation state of carbon (NOSC) or maximal growth rate and the order of substrate depletion. Under soil solution conditions, the growth of Paraburkholderia sp. 1N induced multiauxic substrate depletion patterns that could not be explained by the traditional paradigm of catabolite repression. Importance Exometabolomic footprinting methods have the capability to provide time-resolved observations of the uptake and release of hundreds of compounds during microbial growth. Of particular interest is microbial phenotyping under environmentally relevant soil conditions, consisting of relatively low concentrations and modeling pulse input events. Here we show that growth of a bacterial soil isolate, Paraburkholderia sp. 1N, on a dilute soil extract resulted in a multiauxic metabolic response, characterized by discrete temporal clusters of substrate depletion and metabolite production. Our data did not support the hypothesis that compounds with lower energy content were used preferentially, as each cluster contained compounds with a range of nominal oxidation states of carbon. These new findings with Paraburkholderia sp. 1N, which belongs to a metabolically diverse genera, provide insights on ecological strategies employed by aerobic heterotrophs competing for low-molecular-weight substrates in soil solution.

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Multi-lab EcoFAB study shows highly reproducible physiology and depletion of soil metabolites by a model grass

Cited by 11 publications

References 53 publications

Root morphology and exudate availability is shaped by particle size and chemistry in Brachypodium distachyon

Root morphology and exudate availability is shaped by particle size and chemistry in Brachypodium distachyon

Dynamics in plant roots and shoots minimize stress, save energy and maintain water and nutrient uptake

Ecophysiological Study ofParaburkholderiasp. Strain 1N under Soil Solution Conditions: Dynamic Substrate Preferences and Characterization of Carbon Use Efficiency

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