Water availability as a cross-scale driver of microbial functions and free viral abundance in soil

Viral infection is widespread in natural microbial communities, with extensive study in aquatic ecosystems demonstrating direct influence on host physiology, functional activity, and mortality. While similar dynamics are assumed to occur across ecosystems, soils are distinct microbial habitats where soil physiochemical structure and water availability constrain resource availability. These unique environmental conditions have been widely demonstrated to affect microbial distribution, diversity, and functional activity in bulk soil, while their influence on virus-microbe interactions and free viral abundance remains limited. To address this knowledge gap, this research had three broad aims: i) to investigate variability in microbial responses to drying-rewetting cycles at the scale of aggregate size fractions, ii) to explore potential for aggregate-scale variability in free viral abundance and net virus production rates over time, and iii) to study the influence of dynamic soil drying and rewetting processes on microbial stress responses relative to free viral abundance. Three multifactorial incubation experiments were conducted testing treatment effects of soil aggregate size (Large Macro, Small Macro, and Micro), induction of viral lysis using Mitomycin C (MMC), drying-rewetting processes (i.e., drought length, rewetting frequency), and time. Microbial activity was monitored by repeated sampling of respiration rates with destructive sampling was performed for analysis of dissolved organic carbon, inorganic nitrogen, aggregate stability, activities of hydrolytic extracellular microbial enzymes, and viral particles and bacterial cell abundances. Results from multivariate statistical analysis indicate overarching control of time and water availability on microbial activities, as well as viral abundance and net production rates, across aggregates and in response to induction of viral lysis. In bulk soil, free viral abundance was negatively affected by soil drying and sharply decreased with drying beyond 20% gravimetric water content. Rewetting of dry soil was associated with a burst of microbial activity along with a spike in lytic viral reproduction that increased viral abundance up to 40-fold within 24 h. Together, these findings illustrate the dynamic nature of the responses of soil microbial and viral processes to soil-specific environmental factors at lesser studied spatial and temporal scales.