Interacting Bioenergetic and Stoichiometric Controls on Microbial Growth

Abstract

Microorganisms function as open systems that exchange matter and energy with their surrounding environment. Even though mass (carbon and nutrients) and energy exchanges are tightly linked, there is a lack of integrated approaches that combine these fluxes and explore how they jointly impact microbial growth. Such links are essential to predicting how the growth rate of microorganisms varies, especially when the stoichiometry of carbon- (C) and nitrogen (N)-uptake is not balanced. Here, we present a theoretical framework to quantify the microbial growth rate for conditions of C-, N-, and energy-(co-) limitations. We use this framework to show how the C:N ratio and the degree of reduction of the organic matter (OM), which is also the electron donor, availability of electron acceptors (EAs), and the different sources of N together control the microbial growth rate under C, nutrient, and energy-limited conditions. We show that the growth rate peaks at intermediate values of the degree of reduction of OM under oxic and C-limited conditions, but not under N-limited conditions. Under oxic conditions and with N-poor OM, the growth rate is higher when the inorganic N (NInorg)-source is ammonium compared to nitrate due to the additional energetic cost involved in nitrate reduction. Under anoxic conditions, when nitrate is both EA and NInorg-source, the growth rates of denitrifiers and microbes performing the dissimilatory nitrate reduction to ammonia (DNRA) are determined by both OM degree of reduction and nitrate-availability. Consistent with the data, DNRA is predicted to foster growth under extreme nitrate-limitation and with a reduced OM, whereas denitrifiers are favored as nitrate becomes more available and in the presence of oxidized OM. Furthermore, the growth rate is reduced when catabolism is coupled to low energy yielding EAs (e.g., sulfate) because of the low carbon use efficiency (CUE). However, the low CUE also decreases the nutrient demand for growth, thereby reducing N-limitation. We conclude that bioenergetics provides a useful conceptual framework for explaining growth rates under different metabolisms and multiple resource-limitations.

Bioenergetic control of soil carbon dynamics across depth

“…This is consistent with the idea of SOC becoming increasingly oxidised (less reduced) as decomposition proceed 44 . The γ SOC represents a measure of the chemical energy stored in organic matter, corresponding to the number of electron equivalents per SOC amount 38,43 . The γ SOC is widely known to control microbial carbon-use efficiency 38,45,46 , that is the ratio of growth over C uptake.…”

“…The γ SOC represents a measure of the chemical energy stored in organic matter, corresponding to the number of electron equivalents per SOC amount 38,43 . The γ SOC is widely known to control microbial carbon-use efficiency 38,45,46 , that is the ratio of growth over C uptake. When γ SOC decreases below the degree of reduction of C in biomass of microbial decomposers (γ ~4.2), their biosynthesis become increasingly energy limited.…”

“…We adopted a bioenergetic framework to assess how SOC dynamics could be related to its energy quality for microbial decomposers [25][26][27][28] , defined here as the net energy gain that decomposers could realise for a given energy investment in SOC acquisition. The energy quality of SOC was quantified using the returnon-energy-investment (ROI) parameter 26 , which is the ratio between (i) the energy density of SOC (ΔE, energy content per unit SOC) representing the amount of energy that decomposers could gain by SOC catabolism 38 , and (ii) the mean activation energy (µE a ) of SOC decomposition representing the energetic barriers to its acquisition by decomposers 39 . The energy density of SOC and the activation energy of its decomposition were respectively measured by differential scanning calorimetry and evolved gas analysis during ramped combustion 25,28 .…”

Bioenergetic control of soil carbon dynamics across depth

“…The γ SOC represents a measure of the chemical energy stored in organic matter, corresponding to the number of electron equivalents per SOC amount 38,43 . The γ SOC is widely known to control microbial carbon-use efficiency 38,45,46 , that is the ratio of growth over C uptake. When γ SOC decreases below the degree of reduction of C in biomass of decomposers (γ ~4.2), their biosynthesis become increasingly energy limited.…”

Microbial communities in terrestrial surface soils are not widely limited by carbon

“…Both theory and empirical evidence notably raise a fundamental question: are heterotrophic microbial communities widely limited by soil C, even in C-rich surface soils? According to the principles of matter and energy conservation and ecological stoichiometry (Allen & Gillooly, 2009;Peñuelas & Baldocchi, 2019;Sterner & Elser, 2002), MCL depends on the availability of substrate C relative to other nutrients (generally N and/or P), a notion also supported by many empirical studies, from molecules to ecosystems (Chakrawal et al, 2022;Tamale et al, 2021). The degree of MCL may also be highly variable among substrates due to the broad stoichiometric gradient across diverse C components that range from plant litter to complex soil organic matter (SOM) (Fierer, 2017;Liang et al, 2017;Xu et al, 2013).…”