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 is 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 CRISPR investment 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. These results indicate that 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. Together, these results provide insights into how viral and host communities collectively respond to unpredicted environmental disturbance. HighlightsO_LIIn a seven-year annual study of temperate soils affected by an underground fire, viral communities displayed greater variability across sites (spatial) than over time (temporal). C_LIO_LIViral communities were distinct between heated and unheated soils throughout sampling. C_LIO_LISoil bacterial community composition correlated to viral community composition, though this relationship weakened when accounting for edaphic properties of soil temperature and pH. C_LIO_LISoil viral communities may be less resilient to press disturbance than their host bacterial communities. C_LIO_LIViral-host interactions may shift during soil recovery from long-term heating. C_LI