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Leveraging energy flows to quantify microbial traits in soils
Stockholm University, Faculty of Science, Department of Physical Geography.
Stockholm University, Faculty of Science, Department of Physical Geography.
Number of Authors: 32021 (English)In: Soil Biology and Biochemistry, ISSN 0038-0717, E-ISSN 1879-3428, Vol. 155, article id 108169Article in journal (Refereed) Published
Abstract [en]

Heat dissipation from organic matter decomposition is a well-recognized proxy for microbial activity in soils, but only a few modeling studies have used heat signals to quantify microbial traits such as maximum substrate uptake rate, specific growth rate, mortality rate, and growth efficiency. In this contribution, a hierarchy of coupled mass-energy balance models is proposed to estimate microbial traits encoded in model parameters using heat dissipation and respiration data from glucose induced microbial activity. Moreover, the models are used to explain the observed variability in calorespirometric ratios (CR)-the ratio of heat dissipation to respiration rate. We parametrized four model variants using heat dissipation and respiration rates measured in an isothermal calorimeter during the lag-phase only or during the whole growth-phase. The four variants are referred to as: (i) complex physiological model, (ii) simplified physiological model, (iii) lag-phase model, and (iv) growth-phase model. Model parameters were determined using three combinations of data: A) only the heat dissipation rate, B) only the respiration rate, and C) both heat dissipation and respiration rates. We assumed that the 'best' parameter estimates were those obtained when using all the data (i.e., option C). All model variants were able to fit the observed heat dissipation and respiration rates. The parameters estimated using only heat dissipation data were similar to the 'best' estimates compared to using only respiration rate data, suggesting that the observed heat dissipation rate can be used to constrain microbial models and estimate microbial traits. However, the observed variability in CR was not well captured by some model variants such as the simplified physiological model, in contrast to the lag- and growth-phase model that predicted CR well. This suggests that CR can be used to scrutinize how well metabolic processes are represented in decomposition models.

Place, publisher, year, edition, pages
2021. Vol. 155, article id 108169
Keywords [en]
Calorimetry, Glucose metabolism, Parameter estimation, Microbial activity, Energy balance, Microbial model
National Category
Agriculture, Forestry and Fisheries Biological Sciences
Identifiers
URN: urn:nbn:se:su:diva-193110DOI: 10.1016/j.soilbio.2021.108169ISI: 000626605700014OAI: oai:DiVA.org:su-193110DiVA, id: diva2:1554528
Available from: 2021-05-14 Created: 2021-05-14 Last updated: 2025-01-31Bibliographically 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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