Soil viral community dynamics over seven years of heat disturbance: Spatial variation exceeds temporal in annually sampled soils

Abstract

Viruses are important components of the soil microbiome, influencing microbial population dynamics and the functions of their hosts. However, the relationships and feedbacks between virus dynamics, microbial host dynamics, and environmental disturbance are not understood. Centralia, PA, USA, is the site of an underground coal seam fire that has been burning for over 60 years. As the fire moves along the coal seam, previously heated soils cool to ambient temperature, creating a gradient of heat disturbance intensity and recovery. We examined annual soil viral population dynamics over seven consecutive years in Centralia using untargeted metagenome sequencing. Viral communities changed over time and were distinct between fire-affected and reference sites. Dissimilarity in viral communities was greater across sites (space) than within a site across years (time), and cumulative viral diversity more rapidly stabilized within a site across years than within a year across sites. There also were changes in number of CRISPR arrays per genome as soils cooled, corresponding to shifts in viral diversity. Finally, there were also differences in viral-encoded auxiliary metabolic genes between fire-affected and reference sites. Thus, despite high site-to-site soil viral diversity, there was surprising viral community consistency within a site over the years and shifting host-viral interactions in soils recovering from disturbance. Overall, this work provides insights into the interannual dynamics of soil viruses and their host communities, as well as how they collectively respond to long-term warming.