Efficient assembly and long-term stability of defensive microbiomes via private resources and community bistability

Understanding the mechanisms that promote the assembly and maintenance of host-beneficial microbiomes is an open problem. Empirical evidence supports the idea that animal and plant hosts can combine ‘private resources’ with the ecological phenomenon known as ‘community bistability’ to favour some microbial strains over others. We briefly review evidence showing that hosts can: (i) protect the growth of beneficial strains in an isolated habitat, (ii) use antibiotics to suppress non-beneficial, competitor strains, and (iii) provide resources that only beneficial strains are able to translate into an increased rate of growth, reproduction, or antibiotic production. We then demonstrate in a spatially explicit, individual-based model that these three mechanisms act similarly by selectively promoting the initial proliferation of preferred strains, that is, by acting as a private resource. The faster early growth of preferred strains, combined with the phenomenon of ‘community bistability,’ allows those strains to continue to dominate the microbiome even after the private resource is withdrawn or made public. This is because after a beneficial colony reaches a sufficiently large size, it can resist invasion by parasites without further private support from the host. We further explicitly model localized microbial interactions and diffusion dynamics, and we show that an intermediate level of antibiotic diffusion is the most efficient mechanism in promoting preferred strains and that there is a wide range of parameters under which hosts can promote the assembly of a self-sustaining defensive microbiome. This in turn supports the idea that hosts readily evolve to promote host-beneficial defensive microbiomes.