Local adaptation, geographical distance and phylogenetic relatedness: Assessing the drivers of siderophore‐mediated social interactions in natural bacterial communities

In heterogenous, spatially structured habitats, individuals within populations can become adapted to the prevailing conditions in their local environment. Such local adaptation has been reported for animals and plants, and for pathogens adapting to hosts. There is increasing interest in applying the concept of local adaptation to microbial populations, especially in the context of microbe–microbe interactions. Here, we tested whether cooperation and cheating on cooperation can spur patterns of local adaptation in soil and pond communities of Pseudomonas bacteria, collected across a geographical scale of 0.5 to 50 m. We focussed on the production of pyoverdines, a group of secreted iron‐scavenging siderophores that often differ among pseudomonads in their chemical structure and the receptor required for their uptake. A combination of supernatant‐feeding and competition assays between isolates from four distance categories revealed tremendous variation in the extent to which pyoverdine non‐ and low‐producers can benefit from pyoverdines secreted by producers. However, this variation was not explained by geographical distance, but primarily depended on the phylogenetic relatedness between interacting isolates. A notable exception occurred in local pond communities, where the effect of phylogenetic relatedness was eroded in supernatant assays, probably due to the horizontal transfer of receptor genes. While the latter result could be a signature of local adaptation, our results overall indicate that common ancestry and not geographical distance is the main predictor of siderophore‐mediated social interactions among pseudomonads. We sampled 315 natural isolates of Pseudomonas bacteria from soil (yellow) and pond (blue), and investigated whether pyoverdine non‐ and low‐producers are locally adapted to exploit pyoverdines secreted by producers. We found that the ability to exploit pyoverdines was mainly driven by the phylogenetic relatedness between isolates and not the geographical distance across which isolates were sampled, with one notable exception occurring in local pond communities.