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Interacting Bioenergetic and Stoichiometric Controls on Microbial Growth

Chakrawal, Arjun and Calabrese, Salvatore and Herrmann, Anke and Manzoni, Stefano (2022). Interacting Bioenergetic and Stoichiometric Controls on Microbial Growth. Frontiers in Microbiology , 859063
[Research article]

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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.

Authors/Creators:Chakrawal, Arjun and Calabrese, Salvatore and Herrmann, Anke and Manzoni, Stefano
Title:Interacting Bioenergetic and Stoichiometric Controls on Microbial Growth
Series Name/Journal:Frontiers in Microbiology
Year of publishing :2022
Article number:859063
Number of Pages:18
Publisher:FRONTIERS MEDIA SA
ISSN:1664-302X
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Copyright:Creative Commons: Attribution 4.0
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 2 Engineering and Technology > 209 Industrial Biotechnology > Bioenergy
(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Microbiology (Microbiology in the medical area to be 30109)
Keywords:microbial growth, nitrogen limitation, energy limitation, thermodynamics, bioenergetics, stoichiometry, DNRA, denitrification
URN:NBN:urn:nbn:se:slu:epsilon-p-117409
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-117409
Additional ID:
Type of IDID
DOI10.3389/fmicb.2022.859063
Web of Science (WoS)000804114200001
ID Code:28342
Faculty:NJ - Fakulteten för naturresurser och jordbruksvetenskap
Department:(NL, NJ) > Dept. of Soil and Environment
(S) > Dept. of Soil and Environment
Deposited By: SLUpub Connector
Deposited On:15 Jun 2022 10:28
Metadata Last Modified:15 Jun 2022 10:31

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