Keystone mutualists can facilitate transition between alternative ecosystem states in the soil

Abstract

Symbioses between plants and microbial organisms can fundamentally alter the structure of ecosystems, from their species diversity to rates of nutrient cycling. Yet, many aspects of how differences in the prevalence of microbial symbioses arise are unclear. This is a key knowledge gap, as if co-variation in plant and microbial distributions are primarily determined by extrinsic abiotic factors then symbioses should exert little independent control over ecosystems. To examine the potential for alternative symbiotic communities to arise under similar conditions we examined biogeochemical cycling and microbial community structure in a coastal landscape where historical patterns of vegetation transition are known, allowing us to eliminate abiotic determinism. We found that alternative states in microbial community structure and ecosystem processes emerged under different plant species. Greenhouse studies further demonstrated that plant selection of symbiotic microbes is central to emergence of these alternative states and occurs independent of soil abiotic conditions. Moreover, we provide evidence that transition between states may be highly dependent on the presence of a small set of ruderal symbionts that are rare in mature systems but may act as keystone mutualists. Because differences between these alternative states can be directly linked to plant-microbe symbioses, independent of initial conditions, our results suggesting that biotic feedbacks between keystone symbiotic microbes and plants play a foundational role in the diversity and function of soils.