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Quantifying Microbial Metabolism in Soils Using Calorespirometry — A Bioenergetics Perspective
Stockholm University, Faculty of Science, Department of Physical Geography.ORCID iD: 0000-0003-4572-4347
Stockholm University, Faculty of Science, Department of Physical Geography.
2020 (English)In: Soil Biology and Biochemistry, ISSN 0038-0717, E-ISSN 1879-3428, Vol. 148, article id 107945Article in journal (Refereed) Published
Abstract [en]

Microbial carbon use efficiency (CUE) measures the partitioning between anabolic and catabolic processes. While most work on CUE has been based on carbon (C) mass flows, the roles of organic C energy contents and microbial energy demand on CUE have been rarely considered. Thus, a bioenergetics perspective could provide new insights on how microorganisms utilize C and ultimately allow evaluating their role in C stabilization in soils. Recently, the calorespirometric ratio (CR)— the ratio of heat dissipation and respiration— has been used to characterize the efficiency of microbial growth in soils. Here, we formulate a coupled mass and energy balance model for microbial growth and provide a generalized relationship between CUE and CR. In the model, we consider two types of organic C in soils: an added substrate (e.g., glucose) and the native soil organic matter (SOM), to also account for priming effects. Furthermore, we consider both aerobic and fermentation metabolic pathways. We use this model as a framework to generalize previous formulations and generate hypotheses on the expected variations in CR as a function of substrate quality, metabolic pathways, and microbial traits (specifically CUE). In turn, the same equations can be used to estimate CUE from measured CR. Our results confirm previous findings on CR and show that without microbial growth, CR depends only on the rates of the different metabolic pathways, while CR is also a function of the growth yields for these metabolic pathways when microbial growth occurs. Under strictly aerobic conditions, CUE increases with increasing CR for substrates with a higher degree of reduction than that of the microbial biomass, while CUE decreases with increasing CR for substrates with a lower degree of reduction than the microbial biomass. When aerobic reactions and fermentation occur simultaneously, the relation between CUE and CR is mediated by (i) the degree of reduction of the substrates, (ii) the rates and growth yields of all metabolic pathways, and (iii) the contribution of SOM priming to microbial growth. Using the proposed framework, calorespirometry can be used to evaluate CUE and the role of different metabolic pathways in soil systems.

Place, publisher, year, edition, pages
2020. Vol. 148, article id 107945
Keywords [en]
Bioenergetics, Microbial growth, Calorespirometric ratio, Carbon-use efficiency, Priming effect, Glucose metabolism
National Category
Geosciences, Multidisciplinary
Identifiers
URN: urn:nbn:se:su:diva-185233DOI: 10.1016/j.soilbio.2020.107945ISI: 000566668900051OAI: oai:DiVA.org:su-185233DiVA, id: diva2:1468991
Available from: 2020-09-19 Created: 2020-09-19 Last updated: 2022-02-25Bibliographically approved
In thesis
1. Novel approaches in modeling of soil carbon: Upscaling theories and energetics
Open this publication in new window or tab >>Novel approaches in modeling of soil carbon: Upscaling theories and energetics
2021 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Soils contain more carbon (C) than terrestrial (above ground) and atmospheric carbon combined. Mismanagement of soil C could lead to increased greenhouse gas emissions, whereas practices leading to increased C storage would help mitigate climate change while improving soil fertility and ecological functions. At the center of these complex feedbacks, soil microorganisms play a pivotal role in the cycling of C and nutrients, and thus in soil-climate interactions. However, this role is not fully understood; therefore, developing new methods for studying their dynamics is essential for an understanding of bio-physicochemical processes leading to mineralization or stabilization of soil organic matter (SOM).

Current soil C cycling models lack a robust upscaling approach that links SOM decomposition from process (μm) to observation scale (cm to km). Moreover, these models often neglect energy fluxes from microbial metabolism, which may provide additional constraints in model parameterization and alternative observable quantities such as heat dissipation rate to study decomposition processes. In this doctoral work, I investigated two aspects of microbial processes and their consequences for SOM dynamics: 1) use of energetics to constrain SOM dynamics by explicitly accounting for thermodynamics of microbial growth, and 2) spatial constraints at microscale resulting from the non-uniform distribution of microorganisms and substrates.

In the first part of the thesis, I developed a general mass and energy balance framework for the uptake of added substrates and native SOM. This framework provided the theoretical underpinnings for understanding variations in the calorespirometric ratios—the ratio of rates of heat dissipation to CO2 production—a useful metric used as a proxy for microbial carbon-use efficiency (CUE). Moreover, in a follow-up work, I extended this mass-energy framework to describe dynamic (time-varying) conditions, which was used to interpret rates of heat and CO2 evolution from different soils amended with glucose. The dynamic mass-energy framework was also used as a tool for data-model integration and estimation of microbial functional traits, such as their CUE and maximum substrate uptake rates. In the second part of the thesis, I linked the micro and macroscale dynamics of decomposition using scale transition theory. The findings of this study were further validated from laboratory experiments, in which spatial heterogeneity in the added substrate was manipulated.

Results from the first part show that the calorespirometric ratios can be used to identify active metabolic pathways and to estimate CUE. Further, the heat dissipation rate can be used as a reliable complement or alternative to mass fluxes such as respiration rates for estimating microbial traits and constraining model parameters. In the second part, I show that the co-location of microorganisms and substrates increased, and separation decreased the microbial activity measured as heat dissipation from the incubation experiment. These results were in line with the expectation from the scale transition theory. In summary, this work provides novel approaches for studying soil C cycling and explicitly highlights a way forward to address two fundamental issues in microbial decomposition—the role of spatial heterogeneities and of energetic constraints on microbial metabolisms.

Place, publisher, year, edition, pages
Stockholm: Department of Physical Geography, Stockholm University, 2021. p. 37
Series
Dissertations in Physical Geography, ISSN 2003-2358 ; 18
Keywords
Microorganisms, soil C cycling, spatial heterogeneity, energetics, thermodynamics, microbial metabolism, calorespirometric ratio, microbial traits, heat dissipation, microscale
National Category
Physical Geography Soil Science
Research subject
Physical Geography
Identifiers
urn:nbn:se:su:diva-198898 (URN)978-91-7911-704-7 (ISBN)978-91-7911-705-4 (ISBN)
Public defence
2022-01-14, De Geersalen, Geovetenskapens hus, Svante Arrhenius väg 14 and online via Zoom, the public webinar ID is 665 9022 7507, Stockholm, 14:00 (English)
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Supervisors
Available from: 2021-12-15 Created: 2021-11-23 Last updated: 2022-02-25Bibliographically approved

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Chakrawal, ArjunManzoni, Stefano

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