Structure–function co‐evolution during pedogenesis—Microaggregate development and turnover in soils

Abstract

The development of soil structure and its linkage to functions have become a major research theme boosted by the increasing threat to soil health and fertility due to climate and land-use changes. Water retention, flow of fluids, matter dispersal, habitat provision, nutrient supply, organic matter and element storage are functions of soil fundamental to the life-sustaining ecosystem services. It is well accepted that soil's functions are intimately linked to its architecture and state of aggregation, the void network, and the composition and properties of the solid–fluid biogeochemical interfaces therein (Figure 1). Broad consensus exists that structure develops by the synergistic action of physical, chemical, and biological processes. Inspired by these insights, we see a growing number of research activities that focus on unraveling the intricate interplay and interdependence in search of a theoretical framework that allows for a fundamental understanding of the linkage of structure and function. Substantial progress has been achieved by experimental pedogenesis and the joint application of advanced spectroscopic, microscopic, and tomographic techniques, which enabled studying structure, composition, and biogeochemical interface properties already at the submicron scale. In line with this, modeling endeavors that give feedback to the experimental designs by testing various scenarios serve to explore the factors that govern the co-evolution of structure and function, or challenge concepts in silico, considerably improved over the last decade. This special issue responds to the growing awareness of the importance of the architecture for the functioning of soils and other natural permeable media. We compile recent achievements that shed light on the linkage between soil architecture and functions “from the submicron to the pedon” scale and delineate future research directions. The insights obtained from the various fields of soil research assembled here that employ combinations of experimental, observational, instrumental, and computational methods will certainly allow for a deeper understanding of the intricate pathways of the fascinating co-evolution of structure and function during pedogenesis. There is broad consensus that soil's functions, properties, and traits are intimately linked to its structure, that is, the spatial arrangement of the various organic, inorganic, and biotic components that build the fabric of soil. At what point in time and at what spatial scale this linkage establishes, the pathways of structure development including aggregation, as well as the role that the variety of materials and the diversity of organisms play for the composition, properties, and stability of the structure and its linkage to the functions, have intrigued soil science for decades. This desire for a fundamental understanding also inspired the MADSoil consortium to research this intricate subject with a team that combines empirical, experimental, theoretical, and numerical expertise (Totsche et al., 2018). The coordinated research program was streamlined along the two themes explore and understand: Within explore, MADSoil aimed to characterize the structure, composition, and properties of intact natural and artificial microaggregates with a suite of tomographic, microscopic, and spectroscopic instrumental techniques employed in a joint fashion. This endeavor, however, required the development of novel and sophisticated experimental (e.g., Amelung et al., 2023; Bucka et al., 2019; Dultz et al., 2018; Guhra et al., 2019; Krause et al., 2019; Rodionov et al., 2019; Ritschel et al., 2023) and joint instrumental approaches (e.g., Amelung et al., 2023; Bucka et al., 2021; Felde et al., 2021; Krause et al., 2019). The understand theme aimed to link the structure, composition, and properties of microaggregates to major soil functions—habitat for microorganisms, retention of water, storage of carbon, cycling of elements—by a rigorous mechanistic modeling approach that, again, required the development of appropriate, comprehensive, and operative numerical codes with explanatory power (Guhra et al., 2021; Ray et al., 2017; Ritschel & Totsche, 2019; Ritschel et al., 2018; Rupp et al., 2018; Zech, Ritschel, et al., 2022; Zech, Schweizer, et al., 2022). The research built on the premise that the quality of soil's functions depends on the physicochemical heterogeneity and spatial arrangement of the solid-void interfaces, the so-called biogeochemical interfaces (Totsche et al., 2010), and void network morphology (cf. Rabot et al., 2018) and that the formation and stability of microaggregates originate from molecular interactions of soil compounds that act as aggregate-forming materials and composite building units (Totsche et al., 2018). Based on these suppositions, a set of hypotheses on the formation, stability, and functions of soils at the microscale were devised: Formation of microaggregates. Aggregate formation follows a variety of pathways along deterministic patterns, which are reflected in the composition and spatial arrangement of the microaggregate-forming materials. Minerals like iron oxyhydroxides, phyllosilicate clay minerals, and organic matter including plant and microbial residues act as nuclei for the formation of microaggregates. Stability of microaggregates. The stability of microaggregates is linked to the accumulation and type of organic matter and increases with the amount of pedogenic oxides and fine clay during pedogenesis. Loss of organic matter causes a destabilization of structure by disintegration of aggregates, the release of microaggregates, composite building units, and microaggregate-forming materials, which are then prone to transport or reaggregation. Functions of microaggregates. Soil functions already develop at the scale of microaggregates. The type of mineral nuclei controls the turnover rate of organic matter associated with these minerals. The complexity of microaggregate structure provides different ecological niches that support microbial diversity. The microbial community composition will differ in microaggregates with different nuclei and mineral composition. These hypotheses have been approached by a coordinated effort that combined theoretical expertise and competences from various scientific disciplines, including chemistry, mineralogy, physical chemistry, microbiology, soil physics, data sciences, and numerical modeling. Recent outcomes of this research will be presented in this special issue as a response to the growing awareness of the importance of the three-dimensional build-up, also called architecture, for the functioning of soils and other natural permeable media with special focus on the microscale. MADSoil's research program comprised observational and experimental studies. These were closely linked with theoretical investigations based on numerical simulations of scenarios inspired by our observations and aiming to numerically explore the concepts of understanding (Figure 2). To develop methods for the separation and investigation of microaggregates, we collected topsoil materials from the well-studied field sites in Scheyern, Bavaria, and Rotthalmünster. For the observational studies, we chose field sites that provided combinations of gradients in the contents of the aggregate-forming materials including clay minerals and organic matter. This included an optimization and harmonization step that aimed to optimize the protocol for joint instrumental analysis. With the clay toposequence study, we targeted the formation, architecture, and composition of topsoil microaggregates as a function of microaggregate-forming materials (Biesgen et al., 2020; Krause et al., 2018, 2020; Schweizer et al., 2021). The field studies have been accompanied by dedicated experimental studies. With the multi-stable-isotope labeling experiment, an effort of the full consortium, we were able to follow the aggregation processes over time as a function of the organic gluing agents and inorganic cementing agents with and without the presence of plant roots (Amelung et al., 2023). The experiment included 57Fe-labeled iron-oxihydroxide, 29Si-labeled clay minerals, 13C-labeled extracellular polymeric substances, and a 15N-labeled bacterial strain. With materials collected from the organic matter depletion field trial, the release of microaggregates and their (composite) building units as a function of loss of organic matter and stability were explored. Dedicated experiments focused on the role of soil organic matter (SOM) for the mechanical and physicochemical stability and properties of microaggregates (Roosch et al., 2024, this issue; Siebers et al., 2024, this issue) as well as impacts on soil organic carbon (SOC) storage and aggregation across a rock fragment gradient (Schweizer et al., 2024, this issue). A series of aggregate formation experiments under various conditions with diverse aggregate-forming materials typical for temperate soils (e.g., Bucka et al., 2021; Dultz et al., 2018, 2019, 2021; Guhra et al., 2019; Krause et al., 2019) have been conducted. These were complemented by experimental pedogenesis studies (cf. Bucka et al., 2019; Lehmann et al., 2018; Pronk et al., 2012; Ritschel et al., 2023): The dynamic relocation experiment explored the stability of microaggregates against physicochemical stress under dynamic flow conditions, and the nuclei-framing experiment examined the aggregate formation processes without mechanical disturbance (e.g., Bucka et al., 2019, 2024 [this issue]). Realizing this research approach required the development and advancement of a variety of experimental designs, analytical methods, sample preparation techniques, harmonized protocols for the joint multidisciplinary instrumental analysis and theoretical approaches (Amelung et al., 2024, this issue). Microaggregates in soil are commonly found as part of linings, crusts, or embedded in macroaggregates and even larger aggregated structures in a frequently hierarchical organization. Thus, separating microaggregates from soil is a challenging and delicate effort. For comparative reasons to published results, we established a harmonized protocol for wet separation of aggregate fractions (Krause et al., 2018; Siebers et al., 2018), the common approach to isolate microaggregates. However, wet sieving is known for producing artificial fractions, in particular when combined with sonication. For example, bacterial cells are removed from the mineral surfaces in an uncontrolled manner, thereby precluding the exploration of the original microbial community composition, their biogeography, and thus the relation to the architecture of the microaggregate (Bach et al., 2018; Felde et al., 2021). With this in mind, an alternative dry separation approach was developed, which is based on mechanical crushing in a load frame followed by dry sieving (Felde et al., 2021). With the joint application of tomographic and spectro-microscopic instrumental techniques (Amelung et al., 2024, this issue), the three-dimensional structure of the microaggregates becomes visible (Roosch et al., 2024, this issue). It evolves from the complex spatial arrangement of the diverse aggregate-forming materials that are bound to aggregates by various processes during pedogenesis. Organo–mineral associations, composite building units, and small microaggregates are the building blocks for the aggregate structure of the various soils studied. Aggregation up to the size of macroaggregates was found to be a rather rapid process (hours–weeks), which follows diverse mechanisms in a chronological order (Amelung et al., 2023), and is interrelated with various pedogenetic processes depending on the soil type (Kögel-Knabner & Amelung, 2021). The diverse aggregate-forming materials are arranged in a heterogeneous, random to systematic organized pattern (Lehndorff et al., 2021; Meyer et al., 2024, this issue). Organic matter seems to accumulate in an eventually patchy to piled-up pattern in microaggregates (Schweizer, 2022; Schweizer et al., 2018; Steffens et al., 2017). The variability of components involved in the build-up of aggregates increased with the size of the aggregates, exhibiting a hierarchy in structure with the organo–mineral associations as the smallest compound structures (Figure 3). Various novel pathways including homo- und heteronucleation from soil suspensions (Dultz et al., 2019; Guhra et al., 2019; Krause et al., 2019) and nuclei-framing have been identified (Bucka et al., 2024, this issue). Organic agents of biotic origin were found to be able to initiate and accelerate the aggregation process (Guhra et al., 2024, this issue; Krause et al., 2019). The various pathways resulted in microaggregates with mineral, organic, or no nucleus. The content of clay-sized materials influences the size distribution of the aggregates (Krause et al., 2018; Schweizer et al., 2019) and the carbon stored as occluded particulate organic matter (POM; Schweizer et al., 2021; Tang et al., 2022). The mechanical and water stability of microaggregates was related to organic matter and Fe-speciation (Siebers et al., 2024, this issue). In artificial soils of contrasting texture, Bucka et al. (2024, this issue) studied the aggregate stability using the dry separation approach (Felde et al., 2021). They found that dissolved organic matter caused the formation of water-stable aggregates and shifted the aggregate size distribution toward larger aggregate sizes. However, the mechanical stability was very low and depended on the clay content a to organic matter This with on microaggregates from a natural content along with stability against water no in mechanical (Roosch et al., 2024, this issue). With from the organic matter depletion field trial, to a Siebers et al. (2024, this issue) a of et al. (2024, this issue) found a to aggregate water stability, and Schweizer et al. (2024, this issue) a of organic matter depletion and fractions in the soils with rock The role of soil aggregation for carbon storage was by et al., 2019; et al., which is able to carbon turnover on the Meyer et al. (2024, this issue) that turnover was from in soil to time in microaggregates of a temperate soil However, of the of soil was The structure and of microaggregates to in clay content and type of organic that aggregation is linked to different ecological et al., 2024, this issue). In that the microbial to formation and the formation of gluing agents aggregation in the in a consortium, play a major which is able to gluing agents and thus to Soil organic matter is a complex of and organic of diverse The biotic of plant and and for example, microorganisms, plant and These are involved in pedogenesis in (cf. Guhra et al., for example, by organo–mineral associations or or aggregation et al., et al., They act as separation agents the transport of organo–mineral associations by the or as a gluing thereby aggregate stability and thus et al., 2012; Guhra et al., 2022; et al., the known role of for the of carbon from soil by and et al., et al., 2019; et al., 2020; et al., 2022; et al., 2018), the mechanisms and processes that interactions with other soil have been by Guhra et al. (2024, this issue). They a formation of associations with rather and the role of associations for the storage of The of in the formation and of these fundamental composite building units by the and of soil materials with and These associations are part of the microaggregates, and of the that in of the of in soil and their role in the of organic carbon and from to be on the of and other to soil organic and data on the of their and with aggregation and the formation and of soil structure are required to understand and pedogenesis. 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(2024, this issue) studied the role of dissolved organic matter and soil on turnover and structure formation in an experiment with artificial They found the formation of water-stable aggregates in experimental Aggregation was in with aggregates mechanical stability, retention, microbial and community size were of Within these studies, experimental pedogenesis provides novel experimental approaches for the of pedogenesis also our fundamental understanding of soils research units with in modeling and frequently with an and targeted development of a theoretical and computational a numerical These however, are to theoretical concepts in and to also in complex that is, to on diverse by a of frequently For natural like soil research the various of understanding and be inspired by and the approaches the and experimental To this and to of the concepts and to the we have a approach for development in and research (Figure This approach at the development of numerical for testing concepts and To allow for an eventually research for and to be established that will the of and experimental field and and and the numerical The approach that the of the as well as the scenarios are based on that are inspired by observational data or originate from the experimental studies. The of this process is the and effort the collected expertise and competences of the research It at the of the and in alternative that and the theoretical concepts of the on a This be as the and step in the processes of development and be established as an the growing data and with the concepts will then allow for an of the understanding based on and experimental of Based on the concepts and the to be identified by and the that the and the of a mechanistic is the of the and interactions based on the physical, chemical, and biological the a framework et al., 2017; Ritschel & Totsche, 2019) and the in numerical are the of and outcomes of this approach are for example, in Rupp et al. Guhra et al. or et al. and Zech, Schweizer, et al., 2022). 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(2024, this issue), a of transport and carbon and aggregate turnover that in and turnover of and carbon these studies, modeling was as a to understand the feedback and in the operative across the to a for research that and a for the for a research field including its methods, and to support the processes for research and to for and data under as well as the of the With the rapid progress in soil instrumental analysis at with and (e.g., by joint application of with and soil science is that and with that is, and growing amount of diverse data on the build-up, and functions of The and of in the various fields of soil science has thus become an issue of growing importance for research and Soil research with frequently at intricate and These are in the typical of modeling with artificial that is, based on and however, is the of understanding of the state and of of of or for be based on that physical, chemical, and ecological concepts and are and as their is the are and the are these be and by the of in and in soil With at we will be able to the fundamental and this was modeling thus focus on modeling in the development of and to these build the and interface between and They the of fluids, and thereby the composition, properties, and function of the even to the including the the role of soil's chemical, mineral, and biological diversity and related and is for understanding the functioning of and and thus for the to step in an understanding of the functions with to and cycling is by the application of that is, the of and these approaches with an of the diversity with the and of organic matter in the complex functioning of soils is at Based on the and properties of the diversity and and the biogeochemical processes and element be research thus focus on and matter and cycling in soils with thereby the of and the to explore the diversity and of soil their and their interactions and feedback with the and and land-use are our natural in an Soil and soil carbon element and these life-sustaining ecosystem are linked to the quality of structure and functions of soils that during pedogenesis. With the of and variability in and of two of the factors pedogenesis are in In and and and our In increasing soil by community composition and even on the of our soils will and pathways with for pedogenesis and the functions of for example, carbon element and water Soil aggregate and the microaggregates with the organo–mineral associations, are the major compounds that organic water, an variability of and an microbial diversity. of the pathways or the stability of the soil structure against stress is fundamental for the quality of the functions and for the ecosystem services. for ecosystem and climate and at the and of soils function. will be the fundamental and understanding of the of and climate on pedogenesis and on the of the intricate and complex linkage from the to the and to the scale. the on the to soils functions to its properties has two (cf. Rabot et al., 2018; et al., 2022; & the and the The is to soil structure as the spatial arrangement of that is, and aggregates The other soil structure as the spatial arrangement of the and by the surfaces of the allow for as a of soil structure, and are as of soil in their Rabot et al. to structure as the spatial arrangement of and across different without the heterogeneity of the the heterogeneity and however, to the physicochemical and mechanical properties of the to the void or as an interface between the and biotic like roots and functions like water retention, carbon element of and are by the structure of the void network, the arrangement of the including biotic compounds like and the and heterogeneity of the biogeochemical research thus the and the and heterogeneity of the properties of the and biogeochemical interfaces in soil. It is their physicochemical and mechanical properties that the type and of and thus the interplay of the physical, chemical, and biological mechanisms that are at the of the functions of soil. The MADSoil consortium, which are the Amelung, and the Schweizer, and and the and are for the and during the of research the Formation and turnover of the building blocks of soils We the support of the and are very for the support of and team at special to for and dedicated in the of the research special to Ritschel for and for in our research is to this as no were or during the

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