Host neighborhood shapes bacterial community assembly and specialization on tree species across a latitudinal gradient

Phyllosphere bacterial diversity is shaped through interactions between hosts and microbes. Most studies having focused on pairwise associations between host taxa and their symbionts, little is yet understood about the influence of the host community as a whole in shaping these interactions. Envisioning phyllosphere bacterial communities as a spatially structured network of communities linked by dispersal (i.e., metacommunities) can help us better understand the relative importance of species sorting among host populations and species versus dispersal from the neighboring host community for bacterial community assembly in forest ecosystems. Here we investigate drivers of metacommunity structure of epiphytic bacteria of the phyllosphere among 33 tree host species distributed across a large-scale transition from deciduous to boreal forest. We expect the identity and traits of hosts to play an important role in determining phyllosphere bacterial composition. We further hypothesize that bacterial dispersal from neighboring host species will modulate the match between a focal host species and its microbiota, and shape opportunities for host specialization of phyllosphere bacteria at local and regional scales. We defined specialization as the level of phylogenetic similarity among hosts that a bacterial symbiont associates with. We found that host taxonomic identity and traits were important drivers of bacterial community turnover and variation in host specialization across the landscape. Dispersal from neighboring communities further played a role in homogenizing bacterial communities. The microbiota of focal hosts such as sugar maple was thus increasingly similar to that of neighboring host species along the transition from deciduous to boreal forest. Specialization of bacterial taxa on sugar maple was further positively correlated with the relative abundance of this host in the landscape, revealing a role for the host community context in shaping evolutionary relationships between phyllosphere bacteria and their tree hosts. These results overall suggest that the dispersal of phyllosphere bacteria from the dominant tree community members may be constraining the match between tree species and their symbionts, particularly at their range limits. We also demonstrate that considering host-associated microbial communities as part of metacommunities within the host landscape is a promising tool for improving our understanding of host-symbiont matching.

Automated summary

Phyllosphere bacterial diversity is influenced by interactions between hosts and microbes, with host taxonomic identity and traits being important drivers. Dispersal of bacteria from neighboring communities plays a role in homogenizing bacterial communities and may constrain the match between tree species and their symbionts, particularly at range limits. Considering host-associated microbial communities as part of metacommunities within the host landscape is a promising tool for understanding host-symbiont matching.