Fig 1.
Features included in the microbial degradation model.
(A) Depolymerization dynamics due to activity of exo or endo-enzymes. On the right we show the division of polysaccharides into different classes (from 1 to n) according to their length (N1 representing the concentration of monomers—they all belong to class 1, Ni represents the concentration of a oligomer of size i). Arrows represent possible fluxes between these size classes which result from enzymatic reactions. (B) Microbial growth dynamics, which includes depolymerization of a complex substrate, uptake of small subunits (monomers) and enzyme production. (C) Schematic representation of the spatial grid model, where each microsite represents a microhabitat with a small microbial population. This population can colonize neighboring habitats after its biomass riches a certain threshold.
Fig 2.
Mode of action and distribution of different classes of chitinases.
(A, B) Results of a genetic survey on prevalence of different chitinase classes (KEGG identifiers indicated) within different microbiomes (using Anotree tool—to screen all environments, using JGI—for soils only). (C) Recordings of exo or endo-chitinase activity in chitin degrading microorganisms, the data is based on a literature survey of studies which classified enzyme activity based on reactions with fluorogenic oligomers (details in the S1 Text). We indicate the number of strains used for the classification (total appearances), and the origin of the bacteria (e.g. marine, soil, carnivorous plant etc).
Fig 3.
Differences in the dynamics of release of monomers by exo and endo-enzymes.
(A) Comparison between depolymerization dynamics of exo and endo-enzymes, the system starts with M = 300 nmol/mm3 of monomers all connected into chains of size n = 200 (i.e. the concentration of polymers in the initial pool is Nn(t0) = 1.5 nmol/mm3). Tdeg indicates the time until the available pool of substrate is fully degraded. Note Tdeg is shorter for endo-enzymes. (B) Monomer release by exo- (in concentration Ce = 3 nmol C/mm3) and (C) endo-enzymes (Ce = 3 nmol C/mm3), with same turnover rates kexo = kendo = 0.82 nmol nmol C−1 h−1, for different initial concentrations of polymers (in nmol /mm3) of size n = 200, note the differences in the final amount of monomers obtained. The solid lines in (A, B, C) represent the monomer release dynamics for identical initial pools.
Fig 4.
Growth conditions of endo and exo-enzyme producers.
We show results for degradation of polysaccharide chains of size n = 500 by microorganisms in different set-ups. For comparison, the turnover rates of the two enzymes are the same, kexo = kendo = 0.82 h−1 (A) Maximum biomass (max((Cb(t)) achieved during degradation of different pools of polymers in well mixed conditions. The results show that high substrate amounts hinder the growth of endo-producers and promote the growth of exo-producers. (B) Schematic representation of trade-offs faced by microorganisms. Exo-enzymes can release as many monomers as there are chains available for them to cut, as a consequence exo-enzyme producing microbes starve in the presence of few chains and survive in high substrate conditions. In contrast, endo-enzymes rapidly process low substrate amounts, releasing a high number of monomers. However, in high substrate conditions, since the probability to cut any chain bond is the same, they primarily cleave available chains into oligomers, which cannot be taken up by cells. This can lead to a prolonged absence of monomers, potentially resulting in starvation among endo-enzyme producing microbes.
Fig 5.
Differences between endo and exo-enzyme producers: How much products they lose to diffusion and how they organize in space.
As before we show the results for degradation of polysaccharide chains of size n = 500 by microorganisms in different set-ups. The turnover rates of the two enzymes are the same, kexo = kendo = 0.82 h−1 (A, B) Time evolution of biomass Cb(t) in a single microsite of a spatially explicit model. We assume conditions where microorganisms are unable to divide, but oligomers up to size 10 (see Methods) are able to diffuse. We compare the settings with no diffusion (D0 = 0) and with diffusion (D0 = 30μm2/h). (C, D) Snapshots of the spatial distribution of microbes (biomass concentration Cb(x, y, t)) at indicated times. High substrate concentration: M = 1500 nmol/mm3; Low substrate concentration: M = 150 nmol/mm3.
Fig 6.
Advantages of generalists (producers of both endo and exo-enzymes).
(A, B) Comparison of the total degradation time (Tdeg) of different proportions of exo and endo-enzymes acting simultaneously. The simulation represents only the depolymerization dynamics in the absence of microbes in homogeneous conditions. The complex substrate pool was initiated with a total of 500 nmol/mm3 monomers distributed between chains of n-mers (n indicated in the figure labels). A pool with 3 nmol C/mm3 of two enzymes in different proportions act on the substrate (x-axis and color gradient with purple indicating endo-enzymes and orange indicating exo-enzymes), while the turnover rate or exo-enzyme is kexo = 0.82 h−1, the turnover of endo-enzyme is (A) kendo = kexo and (B) kendo = kexo/2. (C) Maximum biomass reached from different initial concentrations of polymers for microorganisms producing different fractions of endo and exo-enzymes. The parameters are the same as the ones used in simulation in Fig 5, except for the turnover of endo-enzymes, which is kendo = kexo/2. (D, E) Comparison of the maximum growth in the absence of diffusion max() to the maximum growth in the presence of diffusion max(Cb), for different diffusion coefficients D0 for (D) low, M = 150 nmol/mm3, and (E) high substrate, M = 1500 nmol/mm3. Each curve represents a different proportion of exo to endo-enzymes (frexo). Note that for low diffusion the ratios of maximum possible biomass would be the same, and with an increase of diffusion the growth decreases due to loss of soluble oligomers.
Fig 7.
Time evolution of consortia of endo and exo producers: (A) in conditions with high substrate amount initiated with polymer concentration of 1500 nmol/mm3 and (B) with low substrate amount initiated with 150 nmol/mm3. The initial carbon is distributed in chains of size n = 500. Cooperation is only possible when the turnover rates of the two enzyme types are comparable, kexo = kendo = 0.82 h−1. (C) Schematic representation of two interactions within colonies trough the diffusion of degradation products (note that each microsite can be occupied by a single type of microorganism). While endo-producers share more oligomers with their neighbors, exo-producers consume most of the degradation products within a single microsite.
Table 1.
Advantages and downsides of alternative strategies of microorganisms in degradation of complex substrates.