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.

Keywords: agriculture; ecosystem functioning; local adaptation; microbial dispersal; soil bacteria; source–sink models.

Figure 1.

Illustration of some of the hypotheses discussed in the main text. Each panel is a landscape, with different colours indicating different habitat types (agriculture or no agriculture). The landscapes are arranged to illustrate coarse-grained (habitat patch size much larger than dispersal range, left column) and fine-grained (habitat patch size similar to- or smaller than dispersal range, right column) landscapes, as well as landscapes more (bottom row) or less (top row) dominated by intensive agriculture. Bacterial cells are placed across the landscape and the symbol inside represents the habitats to which they are best adapted. (a) Ecotypes are locally adapted to agriculture and non-agriculture environments, as described in hypothesis 1. Owing to the extent of the area under agricultural intensification, genes or species spill over into adjacent non-agriculture areas (hypothesis 2), creating a halo of niche differentiation either of agriculture-adapted strains (hypothesis 3) or introgression of genes selected under agriculture (hypothesis 6). (b) Finer-grained environments select for generalist strains, with adaptations to both agriculture and non-agricultural environments, because both environments are encountered (hypothesis 5). Equivalently, strains with higher dispersal abilities will select for generalist species (hypothesis 4). (c) Increasing the extent of intensive agriculture will result in landscapes dominated by agriculture specialists, because spillover from agriculture swamps locally adapted strains in non-agriculture environments, resulting in a loss of beta diversity (hypothesis 7). (d) The grain of the environment has a weaker effect on bacterial populations when the extent of intensive agriculture is high.