Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments

Abstract

Extracellular enzymes allow microbes to acquire carbon and nutrients from complex molecules and catalyse the rate-limiting step in nutrient mineralization. Because the factors regulating enzyme production are poorly understood, I used a simulation model to examine how competition, nutrient availability and spatial structure affect microbial growth and enzyme synthesis. In simulations where enzyme-producing microbes competed with cheaters (who do not synthesize enzymes but take-up product), higher enzyme costs favoured cheaters, while lower rates of enzyme diffusion favoured producers. Cheaters and producers coexisted in highly organized spatial patterns at intermediate enzyme costs and diffusion rates. Simulations with varying nutrient inputs showed that nitrogen supply can limit carbon mineralization, microbial growth and enzyme production because of the nitrogen-demanding stoichiometry of enzymes (C : N ¼ c. 3.5 : 1). These results suggest that competition from cheaters, slow diffusion and nitrogen limitation may constrain microbial foraging and the enzymatic decomposition of complex compounds in natural environments.

Cooperation and cheating in microbial exoenzyme production – Theoretical analysis for biotechnological applications

“…The first simplification is the restriction to exponentially growing populations.The case of logistic growth eventually leading to stationary phases is left to future extensions of the model.The simplifications allow a largely analytical treatment -the nonlinear dependencies of the initial relative fitness on total cell density and of the equilibrium frequencies on both cell density and the costs can be calculated in closed form. Our results are complementary to, and consistent with, the numerical simulations based on a grid model by Allison [7]. Those simulations predicted that cooperators would outcompete defectors in the case of high benefit, while intermediate benefit leads to coexistence.…”

“…In accordance with the experiment by Greig and Travisano [10] and earlier modeling studies [3,7], here we consider two types of cells only: cooperating cells secreting a given quantity of exoenzyme and complete defectors not secreting any exoenzyme at all. Throughout, the term "enzyme" refers to the extracellular enzyme under study.…”

“…The total production of extracellular enzymes by a population of microorganisms is often diminished by the existence of a subpopulation of nonproducing cells [3,7]. These cells do not invest the metabolic costs of producing and secreting these enzymes, but benefit from the substrates released by the action of the exoenzymes generated by other cells (Fig.…”

Plant-soil interactions and acclimation to temperature of microbial-mediated soil respiration may affect predictions of soil CO2 efflux

“…Manipulations such as sieving breaks up aggregates and makes available previously protected SOM, which increase initial respiration rates, with respect to intact cores (Hartley et al 2007). Strong changes in soil water content (oven drying and rewetting) also affect microbial community composition (Lipson et al 2002;Fierer et al 2003), probably favoring opportunistic species over the endemic community (Allison 2005). This therefore suggests that other experiments should be similarly designed to refute/support our results.…”

Cutting through the complexity of cell collectives

“…In reality, cells benefit from nutrients released into the environment by enzymes as they break down complex substrates into smaller, importable nutrients; however, we only model diffusion of the secreted enzyme. We make this simplification for the sake of clarity and tractability, but note that this approach approximates the full description of any system in which the nutrients liberated by the enzyme diffuse much faster than the enzyme itself [75]. For example, extracellular chitinases of Vibrio spp.…”