Virome responses to heating of a forest soil suggest that most dsDNA viral particles do not persist at 90°C

ABSTRACT Many fundamental characteristics of soil viruses remain underexplored, including the effects of high temperatures on viruses and their hosts, as would be encountered under disturbances like wildland fire, prescribed burning, and soil solarization. In this study, we leveraged three data types (DNase-treated viromes, non-DNase-treated viromes, and 16S rRNA gene amplicon sequencing) to measure the responses of soil viral and prokaryotic communities to heating to 30°C, 60°C, or 90°C, in comparison to field and control conditions. We investigated (1) the response of dsDNA viral communities to heating of soils from two horizons (O and A) from the same forest soil profile, (2) the extent to which specific viral taxa could be identified as heat-sensitive or heat-tolerant across replicates and soil horizons, and (3) prokaryotic and virus-host dynamics in response to heating. We found that both viral and prokaryotic communities responded similarly to the treatment variables. Community composition differed most significantly by soil source (O or A horizon). Within both soil horizons, viral and prokaryotic communities clustered into three groups, based on beta-diversity patterns: the ambient community (field, control, and 30°C samples) and the 60°C and 90°C communities. As DNase-treated viromic DNA yields were below detection limits at 90°C, we infer that most viral capsids were compromised after the 90°C treatment, indicating a maximum temperature threshold between 60°C and 90°C for most viral particles in these soils. We also identified groups of heat-tolerant and heat-sensitive vOTUs across both soil sources. Overall, we found that over 70% of viral populations, like their prokaryotic counterparts, could withstand temperatures as high as 60°C, with shifts in relative abundance explaining most community compositional differences across heating treatments.