Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling

BACKGROUND: As genetic entities infecting and replicating only in bacteria, bacteriophages can regulate the community structure and functions of their host bacteria. The ecological roles of bacteriophages in aquatic and forest environments have been widely explored, but those in agroecosystems remains limited. Here, we used metagenomic sequencing to analyze the diversity and interactions of bacteriophages and their host bacteria in soils from three typical rice agroecosystems in China: double cropping in Guangzhou, southern China, rice–wheat rotation cropping in Nanjing, eastern China and early maturing single cropping in Jiamusi, northeastern China. Enterobacter phage-NJ was isolated and its functions on soil nitrogen cycling and effect on soil bacterial community structure were verified in pot inoculation experiments and 16S rRNA gene sequencing. RESULTS: Soil bacterial and viral diversity and predicted functions varied among the three agroecosystems. Genes detected in communities from the three agroecosystems were associated with typical functions: soil bacteria in Jiamusi were significantly enriched in genes related to carbohydrate metabolism, in Nanjing with xenobiotics biodegradation and metabolism, and in Guangzhou with virulence factors and scarce in secondary metabolite biosynthesis, which might lead to a significant occurrence of rice bacterial diseases. The virus community structure varies significantly among the three ecosystems, only 13.39% of the total viral species were shared by the three rice agroecosystems, 59.56% of the viral species were specific to one agroecosystem. Notably, over-represented auxiliary carbohydrate-active enzyme (CAZyme) genes were identified in the viruses, which might assist host bacteria in metabolizing carbon, and 67.43% of these genes were present in Jiamusi. In bacteriophage isolation and inoculation experiments, Enterobacter bacteriophage-NJ reduced the nitrogen fixation capacity of soil by lysing N-fixing host bacteria and changed the soil bacterial diversity and community structure. CONCLUSION: Our results showed that diversity and function predicted of paddy soil bacteria and viruses varied in the three agroecosystems. Soil bacteriophages can affect nutrient cycling by boosting host metabolism through the carried auxiliary metabolic genes (AMGs) and lysing the host bacteria that are involved in biogeochemical cycles. These findings form a basis for better understanding bacterial and bacteriophage diversity in different rice agroecosystems, laying a solid foundation for further studies of soil microbial communities that support ecofriendly production of healthy rice. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40793-022-00410-8.