Soil aggregates as massively concurrent evolutionary incubators

Soil aggregation, a key component of soil structure, has mostly been examined from the perspective of soil management and the mediation of ecosystem processes such as soil carbon storage. However, soil aggregation is also a major factor to consider in terms of the fine-scale organization of the soil microbiome. For example, the physico-chemical conditions inside of aggregates usually differ from the conditions prevalent in the bulk soil and aggregates therefore increase the spatial heterogeneity of the soil. In addition, aggregates can provide a refuge for microbes against predation since their interior is not accessible to many predators. Soil aggregates are thus clearly important for microbial community ecology in soils (for example, Vos et al., 2013; Rillig et al., 2016) and for microbially driven biogeochemistry, and soil microbial ecologists are increasingly appreciating these aspects of soil aggregation. Soil aggregates have, however, so far been neglected when it comes to evolutionary considerations (Crawford et al., 2005) and we here propose that the process of soil aggregation should be considered as an important driver of evolution in the soil microbial community. There are several features that make soil aggregates specifically interesting, and perhaps even unique, in terms of a setting for microbial evolution (Table 1). Soil aggregation is a continuous and dynamic process in which the formation and disintegration of individual microand macroaggregates are separated in time by periods of relative stability. Each individual soil aggregate may provide a unique environmental compartmentalization of the soil microbial community that is, to a large extent, isolated from its surroundings and that can be thought of as an ‘incubator’ for microbial evolutionary change. Because of their isolation, different aggregates can be regarded as ‘concurrent incubators’ that allow enclosed microbial communities to pursue their own independent evolutionary trajectories during their lifetime (‘incubation period’). The huge number of aggregates that exists at any moment in time validates their conceptualization as ‘massively concurrent incubators’ for microbial evolutionary change (Figure 1). Upon disintegration of soil aggregates (‘incubation cycle ends’), formerly enclosed microbial communities are released and allowed to interact with the microbial community of the soil at large. This combination of features (isolation, large number and relative stability) sets soil aggregates apart from other microbial habitats that may also provide temporary isolation of microbial communities, such as the animal intestinal tract and other parts of the animal body (see also Cordero and Datta, 2016), leaves, roots, and many aquatic habitats (Table 1). However, these habitats do not provide the same combination of extent of isolation, duration of isolation and number of concurrent ‘incubators’ as soil aggregates do. We discuss these specific characteristics of soil aggregates next, before describing how evolutionary change in aggregates can occur and explaining how this system can be tackled empirically.