Microbial dispersal from surrounding vegetation influences phyllosphere microbiome assembly of corn and soybean

Non-crop plants surrounding agricultural fields provide numerous ecological services to crops but have rarely been considered a source of microorganisms during the early stages of crop growth. In this study, we test whether crops in close proximity to surrounding woodland habitat fragments develop a denser microbiome that more closely resembles the microbiome composition of the surrounding vegetation than plants farther away. We sampled epiphytic bacteria from corn and soybean plants weekly for 4 (corn) and 3 (soybean) weeks during early development using a spatially explicit design, and on the final time point, we sampled additional cohorts of younger leaves. To contextualize the source strength of the surrounding vegetation, we also sampled soil at each sampling location. Both crop species exhibited a microbiome density gradient and a decay of microbiome similarity to the surrounding vegetation over a distance of 100 m from the vegetation at many time points. Phyllosphere microbiome similarity to the soil tended to increase into the field interior. The strength of host microbiome filtering also depended on the proximity to the surrounding vegetation, with intermediate to most distant locations exhibiting the highest values of host filtering. Last, the microbiomes of younger leaves tended to more closely resemble those of the older surrounding conspecific leaves than the soil or surrounding woodland vegetation. Overall, our study demonstrates that dispersal of bacteria from nearby leaves can shape the abundance and composition of developing crop phyllosphere microbiomes and highlights the diminishing role that soil plays when plant sources are closer or more abundant.IMPORTANCEA central concern in microbial ecology is understanding the sources of microbial colonists and how proximity to such sources impacts community assembly. This area of research is especially important for plants during early stages of development, where the arrival of leaf-specialized bacteria plays an influential role in priming plant immunity and consequently promoting disease resistance. In this study, we test the effect of dispersal from surrounding vegetation on the phyllosphere assembly of corn and soybean using a time series over the early stages of growth. Our work demonstrates that at these early developmental stages, non-crop vegetation surrounding croplands acts as a meaningful source of phyllosphere microorganisms. We further show that the influence of soil on the phyllosphere depends on host proximity to surrounding vegetation and that microbiomes of young leaves emerging on more mature plants tend to be more influenced by older surrounding crop leaves than soil or non-crop leaves.