Microbial cost of carbon degrading extracellular enzymes: A microcosm and mechanistic modeling approach

Background/Question/Methods: Extracellular enzymes in soils play a key role in carbon mineralization by breaking down complex substrates to simpler compounds which microbes can take up and utilize for metabolism. However, very little is known about the rate of enzyme production by microbial communities. We used a mathematical model and laboratory experiments to determine the rate and cost of enzyme production, and the consequences for growth of two Pseudomonas fluorescens strains. The first strain was a wild-type that produces a casein-digesting protease. The second strain was a mutant that did not produce the protease. These two strains were grown individually and in competition over several days in three media types: glucose, glucose+casamino acids, and glucose+casein. During the experiment CO₂ respiration rates, protease activity, and biomass measurements were taken. The mathematical models were optimized using a Monte Carlo Markov Chain routine and the likelihood of each model was compared using Akaike's Information Criteria (AIC).

Results/Conclusions:

We found clear evidence that, in this system, enzyme production was proportional to microbial uptake as opposed to absolute biomass. We found an enzyme production rate of 0.51±0.02 % of microbial uptake. Enzyme production involved an additional metabolic carbon cost of 1.94±0.05 times the amount of enzyme carbon produced. These costs result in a growth disadvantage for the wild-type strain when in competition with the protease-negative mutant. In soils these growth differences could result in locally oscillating microbial populations as non-enzyme producing variants take over the microbial community, causing reductions in extracellular enzyme production. Enzyme-limited patches could then be taken over again by neighboring microbes that produce enzymes. These dynamics would imply that soil microbial populations are rarely locally stable.