Healthy plants are colonized by microorganisms from the surrounding environment, which form stable communities and provide beneficial services to the host. Culture-independent profiling of the bacterial root microbiota shows that different plant species are colonized by distinct bacterial communities that provide beneficial services to the host. It is, however, not known to what extent the host actively selects these communities and whether commensal bacteria are adapted to a specific plant species. Here, we report a sequence-indexed culture collection from roots and nodules of the model legume Lotus japonicus that contains representatives from the majority of species found in culture-independent profiles. Using taxonomically equivalent synthetic communities from *L. japonicus* and the crucifer *Arabidopsis thaliana* in a multi-species gnotobiotic system, we detect clear signatures of host preference in commensal bacteria in a community context that are indicative of host adaptation. Furthermore, sequential inoculation of either host with synthetic communities reveals strong priority effects during the assembly of the root microbiota, where established communities are resilient to invasion by late-comers. However, our results indicate that host preference by commensal bacteria confers a competitive advantage in their native host. We reveal that host preference is prevalent in commensal bacteria from diverse taxonomic groups and that this trait is directly linked to their invasiveness into standing root-associated communities. Our work has implications for sustainable agriculture through the development of persistent microbial inoculants.
## PRJEB37695
Raw 16S rRNA amplicon reads have been deposited in the European Nucleotide Archive
under the accession number PRJEB37695.
https://www.ebi.ac.uk/ena/browser/view/PRJEB37695
## PRJEB37696
Similarly, sequencing reads and genome assemblies of the Lj-SPHERE core collection have been uploaded to the same database with the accession number PRJEB37696.
