T6SS-mediated competition by Stenotrophomonas rhizophila shapes seed-borne bacterial communities and seed-to-seedling...

Seeds harbor diverse microbial communities important for plant growth and health. During germination, seed exudation triggers intense microbial competition, shaping the communities transmitted to seedlings. This study explores the role of the bacterial type VI secretion system (T6SS)-mediated interference competition in seed microbiota transmission to seedlings. The analysis of T6SS distribution within 180 genome sequences of seed-borne bacterial strains enabled the construction of synthetic communities (SynCom) with different levels of phylogenetic diversity and T6SS richness. These SynComs were inoculated with Stenotrophomonas rhizophila CFBP13503, a bacterial strain possessing an active T6SS in vitro and in planta. The impact of the T6SS on SynCom composition was assessed in vitro by comparing the CFBP13503 wild-type strain or its isogenic T6SS-deficient mutant co-inoculation. Additionally, the effects of the T6SS on bacterial community dynamics during seed-to-seedling transmission were examined following seed inoculation. The T6SS of S. rhizophila CFBP13503 targets a broad range of bacteria belonging to five different orders. The susceptibility of competing bacteria was partly explained by their phylogenetic proximity and metabolic overlap with CFBP13503. Furthermore, the T6SS modulates the relative abundance of specific bacterial taxa during seed-to-seedling transmission depending on the initial seed inoculum and plant developmental stage. Depending on the sensitivity of the co-inoculated competitors, the T6SS can provide a competitive advantage to CFBP13503, resulting in an increase in population size.

The high prevalence of the type VI secretion system (T6SS) in seed-borne bacteria supports the importance of T6SS-mediated competition for seed microbiota assembly. In vitro, S. rhizophila CFBP13503 T6SS exerts a strong impact on bacterial community dynamics. The susceptibility to the T6SS increases with the phylogenetic and metabolic proximities of bacteria to CFBP13503, suggesting the influence of interspecies trophic patterns in T6SS-mediated competitions. In planta and in soil, CFBP13503 T6SS influences specific bacterial taxa, leading to shifts in bacterial interactions and distinct community dynamics. T6SS-mediated competition plays a pivotal role in shaping seed bacterial communities and the dynamics of seed-to-seedling transitions.