Soil microorganisms regulate extracellular enzyme production to maximize their growth rate

Salvatore Calabrese,Ashish A Malik,Binayak P Mohanty

doi:10.1007/s10533-022-00899-8

Salvatore Calabrese, Ashish A Malik + Show 1 more

Open Access

https://doi.org/10.1007/s10533-022-00899-8

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Journal: Biogeochemistry	Publication Date: Feb 14, 2022
Citations: 24	License type: cc-by

Affiliation: University of Aberdeen, Texas A&M University

Abstract

Soil carbon cycling and ecosystem functioning can strongly depend on how microbial communities regulate their metabolism and adapt to changing environmental conditions to improve their fitness. Investing in extracellular enzymes is an important strategy for the acquisition of resources, but the principle behind the trade-offs between enzyme production and growth is not entirely clear. Here we show that the enzyme production rate per unit biomass may be regulated in order to maximize the biomass specific growth rate. Based on this optimality hypothesis, we derive mathematical expressions for the biomass specific enzyme production rate and the microbial carbon use efficiency, and verify them with experimental observations. As a result of this analysis, we also find that the optimal enzyme production rate decays hyperbolically with the soil organic carbon content. We then show that integrating the optimal extracellular enzyme production into soil microbial carbon models may change considerably soil carbon projections under global warming, underscoring the need to improve parameterization of microbial processes.

Highlights

Soil microbial communities play a major role in the biogeochemical cycles of carbon (C) and nutrients in the biosphere (Falkowski et al 2008; Paul 2014; Naylor et al 2020) and their functioning is essential to soil health and fertility (Brady and Weil 2016), and to soil carbon sequestration and, in turn, global warming (Singh et al 2010; Chen et al 2020)
An important aspect of these models is that through the microbial carbon use efficiency (CUE)—the ratio of C used for growth to C acquired— they account for how microbes are allocating C between anabolism, catabolism, and production of extracellular enzymes (Manzoni et al 2012; Sinsabaugh et al 2013; Geyer et al 2016; Manzoni et al 2018)
To test if soil microorganisms regulate their investment in extracellular enzymes so as to maximize their specific growth rate, we checked whether the observations of kE and CUE vary with soil organic carbon (SOC) as predicted by Eqs. 8 and 9, respectively

Summary

Introduction

Soil microbial communities play a major role in the biogeochemical cycles of carbon (C) and nutrients in the biosphere (Falkowski et al 2008; Paul 2014; Naylor et al 2020) and their functioning is essential to soil health and fertility (Brady and Weil 2016), and to soil carbon sequestration and, in turn, global warming (Singh et al 2010; Chen et al 2020). To test if soil microorganisms regulate their investment in extracellular enzymes so as to maximize their specific growth rate, we checked whether the observations of kE and CUE vary with SOC as predicted by Eqs. 8 and 9, respectively. To this regard, we retrieved experimental data from Malik et al (2019), which measured biomass specific enzyme production and carbon use efficiency in circumneutral pH soils from 38 sites across the United Kingdom. This trade-off becomes clearly evident in the negative relationship between CUE and kEopt expressed by Eq 10 (Fig. 4A)

Discussion and implication

Conclusions