Exploring the energetics of soil microbial metabolism under substrate limitation

The growth of soil microorganisms is limited by scarce substrate availability for most of the time in most soils, interrupted only by comparatively brief bursts of activity following localized pulses of substrate input. During periods of starvation, microbes must persist in a state of inactivity or dormancy to maintain their viability. Given the prevalence of such non-growing microbes, the costs of maintenance metabolism as well as those associated with emergence from and return to dormancy can be expected to play a significant role in soil carbon (C) cycling.

Recent advances have highlighted the utility of bioenergetic modeling based on coupled C and energy fluxes for the analysis of microbial activity in soil. In particular, the calorespirometric ratio (CR) of heat to CO₂ production obtained from incubation experiments presents a useful tool for monitoring the bioenergetics of microbial metabolism in a dynamic fashion. However, previous studies have primarily focused on the CR during microbial growth, and the effects of non-growth metabolism are rarely considered.

In this contribution, we present a theoretical analysis of the consequences of non-growth metabolism on temporal patterns of the CR (Fig. 1). Specifically, we employ process-based modeling to show that both exogenous maintenance fueled by the consumption of external substrates and endogenous maintenance fueled by the consumption of biomass have distinct effects on the dynamics of the CR (Fig. 1) as well as on the relationship between CR and microbial C use efficiency (CUE), depending on the energy content of the consumed compounds. To connect these theoretical findings with empirical evidence, we compiled data on the CR measured in unamended soils as well as during the lag and retardation phases of substrate amendment experiments from the literature. The results reveal a wide range of observed CR values consistent with high metabolic diversity of microbial maintenance processes. In addition, we find a strong positive correlation between the non-growth CR and the average SOM energy content in arable soils but observe a weak inverse relationship in forest soils, the causes and implications of which remain to be explored.

Overall, our theoretical findings demonstrate a distinct effect of microbial maintenance metabolism on the coupling between C and energy fluxes in soil, which is supported by existing empirical evidence from incubation experiments.

Fig. 1: Simulated dynamics of CR after addition of labile substrate

both with (red) and without (black) additional utilization of SOM (i.e., priming).

Dotted lines indicate CR calculated from rates of heat and CO₂ release (CR_rate)_,

solid lines indicate CR calculated from cumulative release (CR_cumu).