Soil virus life-strategy conversion and implications for ecosystem and soil functions

Both viral abundance and life state vary across contrasting soil environments and are crucial for mediating microbial metabolism and soil functions. Yet, why soil viruses favor the lytic or lysogenic cycle in a given soil environment, and to what extent they affect soil functions, remains unclear. In this review, we constructed a soil virus abundance dataset containing 691 samples, which for the first time included the lysogenic fraction index to quantify the proportion of soil viruses in the lysogenic state. Moreover, we have assessed the distribution and key drivers of soil viral properties based on 21 soil physicochemical indicators. We also systematically summarized three molecular mechanisms regulating viral lysis-lysogenic transformations that are believed to be widespread in soil environments. We propose a conceptual framework for a transition threshold of viral life strategies based on existing experimental evidence. When environmental stress falls below the critical tolerance level of soil microbes, soil viruses facilitate stress relief. However, once stress exceeds the microbial tolerance threshold, the soil viruses transition to another life cycle, such as from the lysogenic to lytic state. This transition results in completely different effects on microbial metabolic systems and associated soil functions. Further, we documented the role of soil viruses in soil ecosystem functions, highlighting in particular, the importance of the “viral shuttle” and “virovory” mechanisms for soil carbon sequestration and complementary One Health functions. Finally, we provide our perspective on future research needs to advance our understanding of soil virology and its impact on soil functions.