Alternative stable states in soil microbiomes of agroecosystems

Abstract

AbstractArchaea, bacteria, and fungi in the soil are increasingly recognized as major determinants of agricultural productivity and sustainability. Although our knowledge of soil biodiversity has been greatly enhanced for the last decade, defining key characteristics of stable and highly functional microbiomes remains a major challenge. We here show that “stable states” of soil microbiomes can be defined with their disease-suppressive effects on crop plants. We integrated agricultural field metadata with microbial community analyses by targeting > 2,000 soil samples collected across a latitudinal gradient from cool-temperate to subtropical regions, profiling microbiomes constituted, in total, by 11 archaeal, 332 bacterial, and 240 fungal families. A DNA-metabarcoding-based evaluation of balance between prokaryote and fungal abundance indicated that fungus-dominated soil is more resistant to crop plant disease. We then examined whether disease-suppressive soil can be defined based on prokaryote and/or fungal taxonomic compositions. A statistical-physics-based approach for reconstructing “energy landscapes” of community structure indicated that disease-suppressive and disease-susceptible soils could be distinguished as alternative stable states of fungal communities. On the other hand, bacterial community structure could not be classified into a small number of alternative stable states, making it difficult to build simplified criteria for diagnosing disease-suppressive functions of agroecosystems with prokaryote taxonomic compositions alone. As the 22 fungal families keys to define the alternative stable states have cosmopolitan distributions, their roles and compositional balance are potentially keys to maintain agroecosystem functions and stability in diverse types of cropland soils.Significance StatementManaging “healthy” soil microbial communities is a prerequisite of sustainable crop production on the Earth. Based on intensive profiling of soil archaea, bacteria, and fungi in cool-temperate to subtropical regions, we found general community-level characteristics common to disease-resistant agroecosystems. Coexistence of multiple fungal lineages that can suppress devastating pests and pathogens is the key to stabilize and maximize ecosystem functions in agriculture.