Microbes in the Anthropocene: spillover of agriculturally selected bacteria and their impact on natural ecosystems

Abstract

Soil microbial communities are enormously diverse, with at least millions of species and trillions of genes unknown to science or poorly described. Soil microbial communities are key components of agriculture, for example, in provisioning nitrogen and protecting crops from pathogens, providing overall ecosystem services in excess of $1000bn per year. It is important to know how humans are affecting this hidden diversity. Much is known about the negative consequences of agricultural intensification on higher organisms, but almost nothing is known about how alterations to landscapes affect microbial diversity, distributions and processes. We review what is known about spatial flows of microbes and their response to land-use change, and outline nine hypotheses to advance research of microbiomes across landscapes. We hypothesize that intensified agriculture selects for certain taxa and genes, which then ‘spill over’ into adjacent unmodified areas and generate a halo of genetic differentiation around agricultural fields. Consequently, the spatial configuration and management intensity of different habitats combines with the dispersal ability of individual taxa to determine the extent of spillover, which can impact the functioning of adjacent unmodified habitats. When landscapes are heterogeneous and dispersal rates are high, this will select for large genomes that allow exploitation of multiple habitats, a process that may be accelerated through horizontal gene transfer. Continued expansion of agriculture will increase genotypic similarity, making microbial community functioning increasingly variable in human-dominated landscapes, potentially also impacting the consistent provisioning of ecosystem services. While the resulting economic costs have not been calculated, it is clear that dispersal dynamics of microbes should be taken into consideration to ensure that ecosystem functioning and services are maintained in agri-ecosystem mosaics.