Theoretical model uncovering trade-offs faced by bacteria in the decomposition of large oligosaccharides

Microbes play a key role in the degradation of organic matter across all ecosystems. A significant fraction of the organic matter pool available to microorganisms consists of structural polysaccharides, e.g. biopolymers such as cellulose, or chitin, that cannot be directly taken up and have to be broken down outside the cell. For that mean microbes have to produce a variety of extracellular enzymes catalyzing different steps of polymer degradation. Within any substrate-specific enzyme group, e.g. hydrolases that act on a certain polysaccharide such as chitin, we highlight two enzyme types with different kinetic strategies: exo-enzymes that cleave the ends of polysaccharide chains, thereby releasing mono- or dimers, and endo-enzymes that act on all intermittent bonds, thereby generating oligosaccharides of various sizes. Since depolymerization works as a bottleneck for nutrient acquisition and is a multi-step process, the trade-offs of investing in the production of one or the other enzyme type have highly non-trivial consequences for microorganisms. Despite its relevance, the depolymerization dynamics is incorporated in oversimplified manner into microbial growth models, where the general assumption is that all enzymes have exo-like kinetics. In this work we bridge this gap, by theoretically analyzing the consequences of production of different ratios of these enzymes on microbial growth. Our objective was to estimate the possible trade-offs faced by microorganisms growing on biopolymers and compare them to known strategies found in soil bacteria.

To investigate how the interplay of enzyme production strategies within a microbial population affect organic matter degradation, we incorporate polymer degradation by means of population balance equations into an individual-based spatially-explicit microscale microbial community model. This approach allows us to track the spatial distribution of biopolymer molecules of different sizes in space and time, as well as the microbes feeding on them. Our results show that microorganisms are limited not only by the amount of carbon in the system, but also by its form (biopolymer chain size). First we have analysed specialists, producing one or the other enzyme type. We found that the producers of exo-enzymes are well adapted to nutrient rich conditions or when carbon is trapped into small oligomers. We therefore suggest to consider them as copiotrophs. Endo-enzyme producers on the contrary can be considered as oligotrophs, as we found them to thrive in poor nutrient conditions with few long chain molecules. However, endo-producers were completely unable to start growing when too many long chains of nutrients are present. Moreover they are much more susceptible to exploitation as they loose larger parts of their intermediate products to diffusion. For generalists, i.e. microorganisms producing both enzymes, our results show that there is an optimum fraction of endo and exo-enzymes that boosts substrate degradation of long biopolymers and such tuned enzyme production speeds-up microbial growth. Overall, our analysis shows that there are incentive to regulate enzyme production towards this optimum ratio in mixed consortia of cooperating exo and endo-producers.