Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways

Li, Hui; Bölscher, Tobias; Winnick, Matthew J.; Tfaily, Malak M.; Cardon, Zoë G.; Keiluweit, Marco

doi:10.1021/acs.est.0c04592

Cited by 93 publications

(63 citation statements)

References 53 publications

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“…Therefore, the energy required to break these bonds and destabilise organic molecules is also a very important parameter in the control of the MAOM PE. However, while this parameter seems thermodynamically easy to conceptualise, its consideration in PE experiments is still in its infancy (Li et al., 2021).…”

Section: Abiotically Mediated Pe: Concepts and Mechanismsmentioning

confidence: 99%

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Advancing the mechanistic understanding of the priming effect on soil organic matter mineralisation

et al. 2022

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The priming effect (PE) is a key mechanism contributing to the carbon balance of the soil ecosystem. Almost 100 years of research since its discovery in 1926 have led to a rich body of scientific publications to identify the drivers and mechanisms involved. A few review articles have summarised the acquired knowledge; the last major one was published in 2010. Since then, knowledge on the soil microbial communities involved in PE and in PE + C sequestration mechanisms has been considerably renewed. This article reviews current knowledge on soil PE to state to what extent new insights may improve our ability to understand and predict the evolution of soil C stocks. We propose a framework to unify the different concepts and terms that have emerged from the international scientific community on this topic, report recent discoveries and identify key research needs. Seventy per cent of the studies on the soil PE were published in the last 10 years, illustrating a renewed interest for PE, probably linked to the increased concern about the importance of soil carbon for climate change and food security issues. Among all the drivers and mechanisms proposed along with the different studies to explain PE, some are named differently but actually refer to the same object. This overall introduces ‘artificial’ complexity for the mechanistic understanding of PE, and we propose a common, shared terminology. Despite the remaining knowledge gaps, consistent progress has been achieved to decipher the abiotic mechanisms underlying PE, together with the role of enzymes and the identity of the microbial actors involved. However, including PE into mechanistic models of SOM dynamics remains challenging as long as the mechanisms are not fully understood. In the meantime, empirical alternatives are available that reproduce observations accurately when calibration is robust. Based on the current state of knowledge, we propose different scenarios depicting to what extent PE may impact ecosystem services under climate change conditions. Read the free Plain Language Summary for this article on the Journal blog.

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Section: Abiotically Mediated Pe: Concepts and Mechanismsmentioning

confidence: 99%

“…Replacement is promoted by strong ligands such as organic acids, which sorb onto mineral surfaces and displace or release previously sorbed organic compounds from minerals (Li et al, 2021).…”

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confidence: 99%

Advancing the mechanistic understanding of the priming effect on soil organic matter mineralisation

et al. 2022

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“…Plant roots can destabilise SOM associated with minerals via several mechanisms including simple physical disruption, acting as conduits to relieve limiting factors (e.g., oxygen, water, nutrients), and through the specific release of root exudates (Jilling et al, 2018;Keiluweit et al, 2015;Rumpel, 2014;Rumpel & Kögel-Knabner, 2011). Li et al (2021) examined the ability of three exudate types (ligands, reductants and simple sugars) to release carbon from glucose adsorbed to two iron and two aluminium oxides in incubation studies.…”

Section: Soil Structure and Porositymentioning

confidence: 99%

“…The strong ligand, oxalic acid, caused rapid mineralisation by sorption and dissolution of minerals (a direct mobilisation mechanism) whereas the simple sugar, glucose, caused slower mineralisation but increased microbial activity and metabolite production (an indirect microbially-mediated mobilisation mechanism), and the reductant, catechol, promoted both mechanisms (Li et al, 2021). The molecular structure of the carbon compounds in the soil or associated with minerals may also influence the response to inputs of root-derived C. For example, Moore et al (2019) employed mesocosm and modelling studies to demonstrate that complex forms of soil C were more sensitive to root/microbe interactions than simple C structures.…”

Section: Soil Structure and Porositymentioning

confidence: 99%

RUSSELL REVIEW Are plant roots only “in” soil or are they “of” it? Roots, soil formation and function

Gregory

2022

European J Soil Science

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Roots are near-ubiquitous components of soils globally but have often been regarded as separate from the soil rather than a substantial factor in determining what soil is and how it functions. The start of rapid soil formation commenced about 400 million years ago with the emergence of vascular plants and the evolution of roots and associated microbes. Roots and associated microorganisms contribute significantly to soil formation by altering rocks and soil minerals through a variety of biogeochemical processes and supply carbon to a depth that can have long residence times. Living root inputs of carbon via rhizodeposits are more efficient than shoot and root litter inputs in forming slow-cycling, mineral-associated soil organic carbon pools. The current functionality of soils in providing food and fuel and fibres, supplying plant nutrients, filtering water and flood regulation, and disease suppression are all dependent on the activities of plant roots. Roots are actively communicating and collaborating with other organisms for mutual benefit, and the signals underlying this modulation of the rhizosphere microbiome are being identified. In this review I examine how plant roots (an organ not an organism) affect soil formation and function and conclude that, from several perspectives, roots are not just "in" soil but "of" it and that definitions of soil should recognise this. A possible definition is: "Soils are altered surficial rock or sediment, composed of organic matter, minerals, fluids, and organisms whose formation and functionality are influenced by biogeochemical weathering and interactions of these components with plant roots." Highlights • Paleoclimatic and paleosoil research shows the key role of roots and mycorrhiza in soil formation.• Deep roots and living root inputs are substantial contributors to long-term C storage.• Root/microbe signalling facilitates mutualistic symbioses, nutrient uptake and disease suppression.

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“…The interlinked physical, chemical, and biological processes in the rhizosphere combined with the structural heterogeneity of soils are a challenge for the analysis of this complex system. The interaction of root exudates with microbes ( Haichar et al, 2008 ; Zhalnina et al, 2018 ), the effect of exudation on soil structure and aggregation ( Baumert et al, 2018 ), and the association of molecules to minerals ( Keiluweit et al, 2015 ; Li et al, 2021 ) result in a highly variable and permanently changing distribution of molecules. While the direct sampling of root exudates requires artificial – mostly soil-free – conditions ( Phillips et al, 2008 ; Oburger and Jones, 2018 ) the determination of spatial gradients of small and often polar and mobile molecules in the soil cannot be easily achieved by ex situ sampling of exudates.…”

Section: Introductionmentioning

confidence: 99%

Direct Imaging of Plant Metabolites in the Rhizosphere Using Laser Desorption Ionization Ultra-High Resolution Mass Spectrometry

et al. 2021

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The interplay of rhizosphere components such as root exudates, microbes, and minerals results in small-scale gradients of organic molecules in the soil around roots. The current methods for the direct chemical imaging of plant metabolites in the rhizosphere often lack molecular information or require labeling with fluorescent tags or isotopes. Here, we present a novel workflow using laser desorption ionization (LDI) combined with mass spectrometric imaging (MSI) to directly analyze plant metabolites in a complex soil matrix. Undisturbed samples of the roots and the surrounding soil of Zea mays L. plants from either field- or laboratory-scale experiments were embedded and cryosectioned to 100 μm thin sections. The target metabolites were detected with a spatial resolution of 25 μm in the root and the surrounding soil based on accurate masses using ultra-high mass resolution laser desorption ionization Fourier-transform ion cyclotron resonance mass spectrometry (LDI-FT-ICR-MS). Using this workflow, we could determine the rhizosphere gradients of a dihexose (e.g., sucrose) and other plant metabolites (e.g., coumaric acid, vanillic acid). The molecular gradients for the dihexose showed a high abundance of this metabolite in the root and a strong depletion of the signal intensity within 150 μm from the root surface. Analyzing several sections from the same undisturbed soil sample allowed us to follow molecular gradients along the root axis. Benefiting from the ultra-high mass resolution, isotopologues of the dihexose could be readily resolved to enable the detection of stable isotope labels on the compound level. Overall, the direct molecular imaging via LDI-FT-ICR-MS allows for the first time a non-targeted or targeted analysis of plant metabolites in undisturbed soil samples, paving the way to study the turnover of root-derived organic carbon in the rhizosphere with high chemical and spatial resolution.

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Simple Plant and Microbial Exudates Destabilize Mineral-Associated Organic Matter via Multiple Pathways

Cited by 93 publications

References 53 publications

Advancing the mechanistic understanding of the priming effect on soil organic matter mineralisation

Advancing the mechanistic understanding of the priming effect on soil organic matter mineralisation

RUSSELL REVIEW Are plant roots only “in” soil or are they “of” it? Roots, soil formation and function

Direct Imaging of Plant Metabolites in the Rhizosphere Using Laser Desorption Ionization Ultra-High Resolution Mass Spectrometry

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