Substrate traits shape the structure of microbial community engaged in metabolic division of labor

Abstract

Metabolic division of labor (MDOL) is widespread in nature, whereby a complex metabolic pathway is shared between different strains within a community for mutual benefit. However, little is known about how communities engaged in MDOL assemble and spatially organize. We hypothesized that when degradation of an organic compound is carried out via MDOL, substrate concentration and its toxicity modulate the benefit allocation between the two microbial populations, thus governing the assembly of this community. We tested this hypothesis by combining individual-based simulations with pattern formation assays using a synthetic microbial community. We found that while the frequency of the first population increases with an increase in substrate concentration, this increase is capped with an upper bound determined by the biotoxicity of the substrate. In addition, our model showed that substrate concentration and its toxicity affect levels of intermixing between strains. These predictions were quantitatively verified using an engineered system composed of two strains degrading salicylate through MDOL. Our results demonstrate that the structure of the microbial communities can be quantitatively predicted from simple environmental factors, such as substrate concentration and its toxicity, which provides novel perspectives on understanding the assembly of natural communities, as well as insights into how to manage artificial microbial systems.

Even allocation of benefits stabilizes microbial community engaged in metabolic division of labor

“…From this perspective, when designing a synthetic consortium engaged in MDOL for pollutant degradation, it may be useful to assign a by-product to the former populations. Thirdly, our results also showed that if the substrate is toxic, the microbial system will be more stable, which is consistent with the results in our previous study 28 . In summary, our results provide a quantitative way to evaluate the feasibility of applying these strategies into a specific pathway engineering, and thus should greatly assist in designing and managing related artificial microbial systems.…”

“…[8]-[13] in Methods section). Consistent with our previous hypotheses and observations 28 , we next assumed that P, which was produced by the second population, was the sole resource for the growth of both populations, while neither S nor I could be directly used for growth. As a consequence, [0, 1] possesses a preferential access to the final product (P), resulted in a 'private benefit' derived from the product privatization (Figure 1A).…”

“…Another solution to this paradox may be derived from the effects of spatial positioning 46 . Our previous study found that although ‘Embezzler’ strain generally grew more in a two-member microbial colony engaged in MDOL, the second strain is usually not completely excluded 28 , suggesting that specific spatial organizing of a community may facilitate their co-existence. In these spatially structured environments, interaction between the two populations would require their cells to be spatially proximal to each other 49-52 .…”

“…Our synthetic microbial communities were cultured in 25-mL flask containing 5 mL new fresh minimum medium 56 supplemented with naphthalene powder (1% w/v) as the sole carbon source. The biomass and relative fraction were measured using the method described previously 28,57 . The detailed protocols were described in Supplementary information S4.1.6.…”

“…Our recent work combined mathematical modelling and experiments with a synthetic consortium 28 . We found that the traits of the substrate, such as its concentration and toxicity, largely affected the assembly of the MDOL community.…”