Mechanisms of microbiome resilience across scales

Ashley Shade, Department of Microbiology & Molecular Genetics, Michigan State University, East Lansing, MI; Program in Ecology, Evolution and Behavior, Michigan State University, East Lansing, MI; Department of Plant, Soil and Microbial Sciences, Michigan State University, East Lansing, MI

Background/Question/Methods
Microbial communities, also called microbiomes, are front-line functional players in determining system responses to changes in the environment. Microbiomes generally are sensitive to disturbances, which are large changes in the environment. Despite the functional importance of microbiomes, we are just beginning to understand the mechanisms that support their stable performances, especially after disturbances. A mechanistic and predictive understanding of microbiome resilience (the capacity for recovery) is crucial to anticipate how microbial functions will change with global climate change. Here, I develop a conceptual framework to understand how several mechanisms that support microbiome resilience may change in their relative importance across scales, from the level of the individual microbial cell to the level of the planet. I apply Vellend’s synthesis of community ecology and integrate it with concepts from metacommunity theory, community responses in a local environment, and individual plasticity and adaptation, and tailor this framework specifically to microbiome responses with consideration of community structure-function relationships.
Results/Conclusions
I posit that the number of assembly mechanisms at play to support microbiome resilience increase with decreasing scale. A general resilience mechanism is population (demographic) rescue of sensitive microbial populations, which is the “re-seeding” of conspecific microbial cells within the impacted locality. The concept of rescue can be extended to functional rescue when there are functionally equivalent (redundant) taxa. Rescue of microbiome members and functions can be supported by dispersal of identical or functionally equivalent taxa from a regional landscape, and also by reactivation of taxa from the local dormant pool. If the local dormant pool is populated by pre-disturbance contemporaries, these populations are likely to have a local fitness advantage over cells from regionally-dispersed populations. Furthermore, diversification within populations, either via mutations that provide fitness advantages in the disturbed environment or via acquisition of horizontally transferred genes, can promote structural resilience or functional redundancy. My take home message is, first, that population rescue within a microbiome involves assembly processes that interact across multiple scales, and, second, that deterministic reactivation of the local dormant pool has potential as a management strategy to support microbiome resilience.