Microbiome Aggregated Traits and Assembly Are More Sensitive to Soil Management than Diversity

How soil is managed, particularly for agriculture, exerts stresses upon soil microbiomes, resulting in altered community structures and functional states. Understanding how soil microbiomes respond to combined stresses is important for predicting system performance under different land use scenarios, aids in identification of the most environmentally benign managements, and provides insight into how system function can be recovered in degraded soils. We use a long-established field experiment to study the effects of combined chronic (press) disturbance of the magnitude of organic carbon inputs with acute (pulse) effects of physical disturbance by tillage and chemical disturbance due to inorganic fertilization and pesticide application. We show that because of the variety of ways it can be assessed, biodiversity—here based on microbial small subunit rRNA gene phylotypes—does not provide a consistent view of community change. In contrast, aggregated traits associated with soil microbiomes indicate general loss of function, measured as a reduction of average genome lengths, associated with chronic reduction of organic inputs in arable or bare fallow soils and altered growth strategies associated with rRNA operon copy number in prokaryotes, as well as a switch to pathogenicity in fungal communities. In addition, pulse disturbance by soil tillage is associated with an increased influence of stochastic processes upon prokaryote community assembly, but fungicide used in arable soils results in niche assembly of fungal communities compared to untilled grassland. Overall, bacteria, archaea, and fungi do not share a common response to land management change, and estimates of biodiversity do not capture important facets of community adaptation to stresses adequately. IMPORTANCE Changes in soil microbiome diversity and function brought about by land management are predicted to influence a range of environmental services provided by soil, including provision of food and clean water. However, opportunities to compare the long-term effects of combinations of stresses imposed by different management approaches are limited. We exploit a globally unique 50-year field experiment, demonstrating that soil management practices alter microbiome diversity, community traits, and assembly. Grassland soil microbiomes are dominated by fewer—but phylogenetically more diverse—prokaryote phylotypes which sustain larger genomes than microbiomes in arable or bare fallow soil maintained free of plants. Dominant fungi in grassland soils are less phylogenetically diverse than those in arable or fallow soils. Soil tillage increases stochastic processes in microbiome assembly: this, combined with reduced plant biomass, presents opportunities for organisms with a capacity for pathogenesis to become established in stressed soils.