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Soil microorganisms regulate extracellular enzyme production to maximize their growth rate

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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.

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Data availability

The original data used in this paper can be found in Malik et al. (2018, 2019).

Code availability

Processed data and the Mathematica code used to draw the Figures is available at https://doi.org/10.4211/hs.7ada4439903f4156be3143e36a9693c7 under a Creative Common Attribution CC-BY.

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Acknowledgements

We gratefully acknowledge support by the Department of Biological and Agricultural Engineering and AgriLife Research at Texas A&M University, and the USDA National Institute of Food and Agriculture.

Funding

This work was supported by the Department of Biological and Agricultural Engineering and AgriLife Research at Texas A&M University, and the USDA National Institute of Food and Agriculture, Hatch project 1023954 and multi-state Hatch Project W-4188.

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Authors and Affiliations

  1. Department of Biological and Agricultural Engineering, Texas A&M University, 400 Bizzell St, College Station, TX, 77843, USA

    Salvatore Calabrese & Binayak P. Mohanty

  2. School of Biological Sciences, University of Aberdeen, Aberdeen, AB24 3UU, UK

    Ashish A. Malik

Authors
  1. Salvatore Calabrese
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  2. Binayak P. Mohanty
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  3. Ashish A. Malik
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Contributions

Conceptualization: SC; Methodology: SC, BM, AAM; Formal analysis and investigation: SC, BM, AAM; Writing - original draft preparation: SC; Writing - review and editing: SC, BM, AAM. Funding acquisition: SC.

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Correspondence to Salvatore Calabrese.

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The authors declare no conflicts of interest.

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Responsible Editor: Justin B. Richardson.

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Calabrese, S., Mohanty, B.P. & Malik, A.A. Soil microorganisms regulate extracellular enzyme production to maximize their growth rate. Biogeochemistry 158, 303–312 (2022). https://doi.org/10.1007/s10533-022-00899-8

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

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