T4-like Phages Reveal the Potential Role of Viruses in Soil Organic Matter Mineralization

Viruses are the most abundant biological entities in the world, but their ecological functions in soil are virtually unknown. We hypothesized that greater abundance of T4-like phages will increase bacterial death and thereby suppress soil organic carbon (SOC) mineralization. A range of phage and bacterial abundances were established in sterilized soil by reinoculation with 10^-3 and 10^-6 dilutions of suspensions of unsterilized soil. The total and viable 16S rRNA gene abundance (a universal marker for bacteria) was measured by qPCR to determine bacterial abundance, with propidium monoazide (PMA) preapplication to eliminate DNA from non-viable cells. Abundance of the g23 marker gene was used to quantify T4-like phages. A close negative correlation between g23 abundance and viable 16S rRNA gene abundance was observed. High abundance of g23 led to lower viable ratios for bacteria, which suggested that phages drove microbial necromass production. The CO₂ efflux from soil increased with bacterial abundance but decreased with higher abundance of T4-like phages. Elimination of extracellular DNA by PMA strengthened the relationship between CO₂ efflux and bacterial abundance, suggesting that SOC mineralization by bacteria is strongly reduced by the T4-like phages. A random forest model revealed that abundance of T4-like phages and the abundance ratio of T4-like phages to bacteria are better predictors of SOC mineralization (measured as CO₂ efflux) than bacterial abundance. Our study provides experimental evidence of phages' role in organic matter turnover in soil: they can retard SOC decomposition but accelerate bacterial turnover.