Plant-pathogen interactions are shaped by multiple environmental factors, making it difficult to predict disease dynamics even in relatively simple agricultural monocultures. Here, we explored how variation in the initial soil microbiome predicts future disease outcomes at the level of individual plants. We found that the composition and functioning of the initial soil microbiome predetermined whether the plants survived or succumbed to disease. Surviving plant microbiomes were associated with specific rare taxa, highly pathogen-suppressing Pseudomonas and Bacillus bacteria, and high abundance of genes encoding antimicrobial compounds. Microbiome-mediated plant protection could subsequently be transferred to the next plant generation via soil transplantation. Together, our results suggest that small initial variation in soil microbiome composition and functioning can determine the outcomes of plant-pathogen interactions under natural field conditions.

Host-associated bacterial communities can function as an important line of defence against pathogens in animals and plants. Empirical evidence and theoretical predictions suggest that species-rich communities are more resistant to pathogen invasions. Yet, the underlying mechanisms are unclear. Here, we experimentally test how the underlying resource competition networks of resident bacterial communities affect invasion resistance to the plant pathogen Ralstonia solanacearum in microcosms and in tomato plant rhizosphere. We find that bipartite resource competition networks are better predictors of invasion resistance compared with resident community diversity. Specifically, communities with a combination of stabilizing configurations (low nestedness and high connectance), and a clear niche overlap with the pathogen, reduce pathogen invasion success, constrain pathogen growth within invaded communities and have lower levels of diseased plants in greenhouse experiments. Bacterial resource competition network characteristics can thus be important in explaining positive diversity–invasion resistance relationships in bacterial rhizosphere communities.

Bacterial communities associated with plant roots play an important role in the suppression of soil-borne pathogens, and multispecies probiotic consortia may enhance disease suppression efficacy. Here we introduced defined Pseudomonas species consortia into naturally complex microbial communities and measured the importance of Pseudomonas community diversity for their survival and the suppression of the bacterial plant pathogen Ralstonia solanacearum in the tomato rhizosphere microbiome. The survival of introduced Pseudomonas consortia increased with increasing diversity. Further, high Pseudomonas diversity reduced pathogen density in the rhizosphere and decreased the disease incidence due to both intensified resource competition and interference with the pathogen. These results provide novel mechanistic insights into elevated pathogen suppression by diverse probiotic consortia in naturally diverse plant rhizospheres. Ecologically based community assembly rules could thus play a key role in engineering functionally reliable microbiome applications. IMPORTANCE The increasing demand for food supply requires more-efficient control of plant diseases. The use of probiotics, i.e., naturally occurring bacterial antagonists and competitors that suppress pathogens, has recently reemerged as a promising alternative to agrochemical use. It is, however, still unclear how many and which strains we should choose for constructing effective probiotic consortia. Here we present a general ecological framework for assembling effective probiotic communities based on in vitro characterization of community functioning. Specifically, we show that increasing the diversity of probiotic consortia enhances community survival in the naturally diverse rhizosphere microbiome, leading to increased pathogen suppression via intensified resource competition and interference with the pathogen. We propose that these ecological guidelines can be put to the test in microbiome engineering more widely in the future.

Accumulating evidence suggests that the response of bacteria to antibiotics is significantly affected by the presence of other interacting microbes. These interactions are not typically accounted for when determining pathogen sensitivity to antibiotics. In this perspective, we argue that resistance and evolutionary responses to antibiotic treatments should not be considered only a trait of an individual bacteria species but also an emergent property of the microbial community in which pathogens are embedded. We outline how interspecies interactions can affect the responses of individual species and communities to antibiotic treatment, and how these responses could affect the strength of selection, potentially changing the trajectory of resistance evolution. Finally, we identify key areas of future research which will allow for a more complete understanding of antibiotic resistance in bacterial communities. We emphasise that acknowledging the ecological context, i.e. the interactions that occur between pathogens and within communities, could help the development of more efficient and effective antibiotic treatments.