Biotic and abiotic factors distinctly drive contrasting biogeographic patterns between phyllosphere and soil resistomes in natural ecosystems

The phyllosphere and soil are two of the most important reservoirs of antibiotic resistance genes (ARGs) in terrestrial ecosystems. However, comparative studies on the biogeographic patterns of ARGs in these two habitats are lacking. Based on the construction of ARG abundance atlas across a > 4,000 km transect in eastern and northern Australia, we found contrasting biogeographic patterns of the phyllosphere and soil resistomes, which showed their distinct responses to the biotic and abiotic stresses. The similarity of ARG compositions in soil, but not in the phyllosphere, exhibited significant distance-decay patterns. ARG abundance in the phyllosphere was mainly correlated with the compositions of co-occurring bacterial, fungal and protistan communities, indicating that biotic stresses were the main drivers shaping the phyllosphere resistome. Soil ARG abundance was mainly associated with abiotic factors including mean annual temperature and precipitation as well as soil total carbon and nitrogen. Our findings demonstrated the distinct roles of biotic and abiotic factors in shaping resistomes in different environmental habitats. These findings constitute a major advance in our understanding of the current environmental resistomes and contribute to better predictions of the evolution of environmental ARGs by highlighting the importance of habitat difference in shaping environmental resistomes.