Associational effects in the microbial neighborhood

Abstract

Even though "perfect" metagenomes or metatranscriptomes are close at hand, the implicit assumption of spatial homogeneity in the "omic" approaches makes it difficult if not impossible to relate those data to ecological processes occurring in natural and man-made ecosystems. In fact, the distribution of microbes in their habitats is far from being uniform and random. Microbial communities show a high degree of spatial organization that stems from environmental gradients and local interactions. These interactions can be very complex and may involve multiple species. Several studies highlighted the importance of indirect interactions for community stability, but the absence of a theoretical framework for microbial ecology restricts the possibilities to strike a balance between the investigation of simple communities with purely pairwise interactions and the attempts to understand interaction patterns in whole communities based on meta-omics studies. Here we suggest adapting the concept of Associational Effects (AE) from plant ecology, to better understand the link between ecological interactions, spatial arrangement, and stability in microbial communities. By bringing together a conceptual framework developed for plants and observations made for microbes, this perspective article fosters synthesis of related disciplines to yield novel insights into the advancing field of spatial microbial ecology. To promote the integration into microbial ecology, we (i) outline the theoretical background of AE, (ii) collect underlying mechanisms by literature synthesis, (iii) propose a three-point roadmap for the investigation of AE in microbial communities, and (iv) discuss its implications for microbial ecology research.

Fig. 1

Transfer of the AE framework from plant to microbial ecology. The framework describes the modulation of the interaction between a plant and a herbivore by a neighboring plant species. The modulation depends on the spatial organization and can either decrease (Associational Resistance, AR) or increase (Associational Susceptibility, AS) the damage/mortality of the focal species. In microbial ecology, this concept will help to bundle research activities on indirect interactions in spatially structured microbial communities

Fig. 2

Physical, chemical, and biological mechanisms causing AE in bacterial communities. Physical mechanisms mainly prevent the accessibility or ingestion of the focal species (F) by forming larger or more complex structures together with the modulating species (M). Chemical mechanisms lead to repellence or attraction of predators via the production and release of secondary metabolites by M, whereas the detoxification of chemicals by M decreases the susceptibility of F. Biological mechanisms are diverse and include changes in the abundance or traits of F, or the attraction of natural enemies by M

Fig. 3

Conceptual, experimental, and methodological demands to study AE in microbial communities. Although direct pairwise interactions were intensively studied, the importance of indirect interactions in microbial ecology remains elusive. To move beyond communities with simple pairwise interactions, it requires (i) a rethinking of existing theories and concepts, (ii) tailored experimental systems to study microbial interactions in spatially structured assemblies and habitats, and (iii) new modeling approaches considering higher-order interactions in spatially explicit modeling environments