A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes

Abstract

Microbial communities can be considered complex adaptive systems. Understanding how these systems arise from different components and how the dynamics of microbial interactions allow for species coexistence are fundamental questions in ecology. To address these questions, we built a three-species synthetic community, called BARS (Bacillota A + S + R). Each species in this community exhibits one of three ecological roles: Antagonistic, Sensitive, or Resistant, assigned in the context of a sediment community. We show that the BARS community reproduces features of complex communities and exhibits higher-order interaction (HOI) dynamics. In paired interactions, the majority of the S species (Sutcliffiella horikoshii 20a) population dies within 5 min when paired with the A species (Bacillus pumilus 145). However, an emergent property appears upon adding the third interactor, as antagonism of species A over S is not observed in the presence of the R species (Bacillus cereus 111). For the paired interaction, within the first 5 min, the surviving population of the S species acquires tolerance to species A, and species A ceases antagonism. This qualitative change reflects endogenous dynamics leading to the expression for tolerance to an antagonistic substance. The stability reached in the triple interaction exhibits a nonlinear response, highly sensitive to the density of the R species. In summary, our HOI model allows the study of the assembly dynamics of a three-species community and evaluating the immediate outcome within a 30 min frame. The BARS has features of a complex system where the paired interactions do not predict the community dynamics. The model is amenable to mechanistic dissection and to modeling how the parts integrate to achieve collective properties.