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Research article - Peer-reviewed, 2022

Interacting Bioenergetic and Stoichiometric Controls on Microbial Growth

Chakrawal, Arjun; Calabrese, Salvatore; Herrmann, Anke M.; Manzoni, Stefano

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 (N-Inorg)-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 N-Inorg-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.

Keywords

microbial growth; nitrogen limitation; energy limitation; thermodynamics; bioenergetics; stoichiometry; DNRA; denitrification

Published in

Frontiers in Microbiology
2022, article number: 859063
Publisher: FRONTIERS MEDIA SA

Authors' information

Chakrawal, Arjun
Stockholm University
Calabrese, Salvatore
Texas AandM University College Station
Swedish University of Agricultural Sciences, Department of Soil and Environment
Manzoni, Stefano
Stockholm University

UKÄ Subject classification

Microbiology
Bioenergy

Publication Identifiers

DOI: https://doi.org/10.3389/fmicb.2022.859063

URI (permanent link to this page)

https://res.slu.se/id/publ/117409