Quantifying microbial metabolism in soils using calorespirometry — A bioenergetics perspective

Arjun Chakrawal,Anke M Herrmann,Hana Šantrůčková,Stefano Manzoni

doi:10.1016/j.soilbio.2020.107945

Abstract

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.

Highlights

Soil organic matter (SOM) provides both energy and materials for biosynthesis to soil microorganisms
To interpret the observed variability of calorespirometric ratio (CR) in soils, we formulated a modeling framework based on previously existing bioenergetic theories (Roels, 1980a; Hansen et al, 2004; Von Stockar et al, 2006)
Our framework shows that combined aerobic and fermentation pathways for substrate metabolism can contribute to the observed variation in CR from soils

Summary

Introduction

Soil organic matter (SOM) provides both energy (catabolism) and materials for biosynthesis (anabolism) to soil microorganisms. Microbial carbon use efficiency (CUE)—the ratio of C used for biosynthesis over C consumed—measures how much of the C used by microbes is routed to anabolic reactions, and remains in the soil (Cotrufo et al, 2013; Manzoni et al, 2018). This efficiency concept is not new, as its origin can be traced back to studies on microbial growth in the late 1940s (Monod, 1949). Because the drivers and variability of CUE are still not fully understood, finding methods to quantify CUE reliably across systems and experimental setups is important

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