Quantitative and Dynamic Properties of Nutrient Colimitation in Microbial Populations

Academic Background

The growth, physiology, and metabolic activity of microorganisms are fundamentally controlled by resource availability. Understanding which resources limit microbial growth and to what extent is not only a core concept in microbiology but also crucial for predicting microbial contributions to biogeochemical cycles, inhibiting pathogens in the human body, and cultivating microbes in biotechnology. While individual limiting resources can be studied in isolation, there is evidence that microorganisms are often simultaneously limited by multiple resources, a phenomenon known as “nutrient colimitation.” However, due to the lack of quantitative measures for nutrient colimitation and systematic tests of resource conditions, existing data are difficult to interpret and compare. Therefore, the authors propose a hypothesis: microorganisms frequently experience nutrient colimitation in both laboratory and natural settings, and nutrient colimitation is a continuous state that can dynamically change with resource conditions.

Source of the Paper

This paper was co-authored by Noelle A. Held, Aswin Krishna, Donat Crippa, Rachana Rao Batta, Alexander J. Devaux, Anastasia Dragan, and Michael Manhart, affiliated with the Swiss Federal Institute of Technology (ETH Zurich), the Swiss Federal Institute of Aquatic Science and Technology (Eawag), the University of Southern California, and Rutgers University. The paper was published on December 18, 2024, in the Proceedings of the National Academy of Sciences (PNAS).

Research Process

1. Quantitative Theoretical Framework for Nutrient Colimitation

The authors first proposed a quantitative theoretical framework to describe the continuum of resource colimitation states and how these states dynamically change with resource conditions. This framework goes beyond the traditional “Law of the Minimum,” which states that growth is solely determined by the resource that is most scarce relative to biological demand. By defining “limitation coefficients,” the authors quantified the extent to which each resource limits growth rate and introduced the “effective number of limiting processes” as a metric for colimitation.

2. Experimental Validation: Colimitation in Escherichia coli

To validate this theory, the authors chose Escherichia coli as a model organism and investigated the colimitation of glucose and ammonium on the growth rate and yield of E. coli under laboratory conditions. By systematically scanning different concentrations of glucose and ammonium, the authors measured the growth rate and yield of E. coli and analyzed the data to determine the extent of colimitation.

3. Environmental Data Analysis: Colimitation in Natural Ecosystems

To further validate the prevalence of colimitation in nature, the authors analyzed microbial growth data from various natural ecosystems. By collecting data on the half-saturation concentrations of resources and their environmental concentrations across different organisms and environments, the authors estimated the extent to which these resources limit microbial growth and found that colimitation is widespread in marine, freshwater, and gut microbiomes.

Key Findings

1. Colimitation in Escherichia coli

Experimental results showed that E. coli exhibits significant colimitation of glucose and ammonium under typical laboratory conditions (e.g., M9 medium). Growth rate and yield were limited by different resources, and the extent of colimitation varied with resource concentrations. By fitting different growth models, the authors found that colimitation models (e.g., the Poisson arrival time model) better explained the experimental data than non-colimitation models (e.g., the Blackman model).

2. Colimitation in Natural Ecosystems

Analysis of environmental data revealed that many marine microorganisms exhibit significant colimitation of resources such as phosphate, nitrate, and ammonium. Freshwater and gut microorganisms showed lower levels of colimitation, but it was still present. Through quantitative analysis, the authors demonstrated the continuity and prevalence of colimitation in nature.

Conclusions

This study presents a quantitative framework for understanding and quantifying nutrient colimitation in microbial populations in biogeochemical, biotechnological, and human health contexts. The results indicate that nutrient colimitation is a common phenomenon in microbial growth, and the extent of colimitation can dynamically change with resource conditions. This framework provides a theoretical foundation for future research on colimitation in natural systems and offers new tools for predicting and controlling microbial growth in environmental, biotechnological, and clinical settings.

Research Highlights

1. Quantitative Framework: A quantitative theoretical framework was proposed to describe and quantify nutrient colimitation in microorganisms, moving beyond the traditional “Law of the Minimum.”
2. Experimental Validation: Systematic experiments demonstrated significant colimitation of glucose and ammonium in E. coli under laboratory conditions.
3. Environmental Data Analysis: Analysis of microbial growth data from natural ecosystems revealed the prevalence and continuity of colimitation in nature.
4. Practical Applications: This framework provides new tools and methods for predicting and controlling microbial growth in environmental, biotechnological, and clinical contexts.

Additional Valuable Information

The study also explored the potential impacts of colimitation on microbial physiology, ecology, and evolution, and proposed future research directions, including systematic scans of natural systems to estimate the extent of colimitation and identifying the molecular mechanisms underlying colimitation. These studies will contribute to a deeper understanding of microbial growth and competition strategies in natural environments.