Unearthing Diversity and Activity Patterns of Bacteriophage Communities in an Agricultural Soil Ecosystem

Abstract:

Frequent cropping of agricultural plant species in short rotations has been associated with an observed decline in crop yield. As such, there is interest in examining the potential role of soil-dwelling microbial species on this phenomenon. In particular, there is very little known about the diversity, distribution and activity of bacteriophage communities in agricultural soil ecosystems.

Phages were identified from three libraries: bacterial metagenomes, DNA viromes and RNA-seq libraries, generated from soil samples taken from fields of Oilseed Rape (Brassica napus). Viral community diversity was described and compared between two crop rotation strategies and across two soil compartments. A complementary transcriptomic dataset was used to describe the activity of these viral communities at three time points across the agricultural year.

We identified a large number of novel dsDNA phage populations, and expanded on the known number of ssRNA phages by over 10 times. Compositional differences were observed in phage communities between the crop rotation strategies and across soil compartments, such that few phages were shared across all soil samples, and most were sample-specific. Further, we described the variance in viral gene expression across samples, showing greatest viral activity in the bulk soil, moderate activity in the rhizosphere, and low activity at the plant roots. Putative auxiliary metabolic genes associated with carbon and nitrogen cycling in the soil, including chitinase and isocitrate lyase, were found to be differentially expressed in a rotation and compartment-specific manner.

Our results describe novel phage communities comprising dsDNA and ssRNA phages, and demonstrate distinctive compositional, abundance and gene expression profiles across crop rotation and soil compartment for the first time. Whilst the function of these soil phage communities requires more research, our results show high phage activity, including the expression of auxiliary metabolic genes integral to carbon and nitrogen cycling.

We have described, for the first time, how phage community diversity, distribution and activity vary between crop rotation strategies and across soil compartments in an agricultural soil ecosystem.