Biogeographic patterns of viral communities, ARG profiles and virus-ARG associations in adjacent paddy and upland soils across black soil region

Abstract

Biogeographic distribution of prokaryotic and eukaryotic communities has been extensively studied. Yet, our knowledge of viral biogeographic patterns, the corresponding driving factors and the virus-resistome associations is still limited. Here, using metagenomic analysis, we explored the viral communities and profiles of antibiotic resistance genes (ARGs) in 30 fields of paddy (rice soils, RS) and upland soils (corn soils, CS) at a regional scale across black soil region of Northeast China. Our finding revealed that viral communities displayed significant distance-decay relationships, and environmental variables largely dominated viral community patterns in agricultural soils. Compared to RS, viral community in CS harbored significantly higher viral α-diversity and distinct β-diversity, and exhibited a higher turnover along with environmental gradients and spatial distance. However, no clear latitudinal diversity gradient (LDG) pattern was observed in viral diversity over large-scale sampling for RS and CS, and heterogeneous distribution of soil viruses was well maintained over large-scale sampling. Soil pH was the important influential factor driving viral community, and the high soil nutrient levels negatively affected viral diversity. Uroviricota, Nucleocytoviricota and Artverviricota were the main viral phyla in agricultural soils, and virus-host linkages spanned 17 prokaryotic phyla, including Actinobacteriota and Proteobacteria. Besides, 2,578 ARG subtypes were retrieved and conferred resistance to 27 types of antibiotics, in which multidrug was the predominant ARG type in Mollisols. Procrustes analysis showed the significant contribution of viral community to ARG profiles, which was more obvious in CS compared to RS. We identified 9.61% and 11.4% of soil viruses carried at least one ARG can infect multi-host in RS and CS. Furthermore, 43 and 77 complete viral metagenome-assembled genome (vMAG) were reconstructed in RS and CS, respectively. Notably, the lysogenic phages in RS contained 29.7% of ARGs, a higher proportion than the 12.5% found in CS. Overall, our study underscored the prevalent distribution of viral communities and ARG profiles at a large spatial scale, and the distinct ecological strategies of virus-ARG associations in adjacent paddy and upland soils.