Viruses in soil: Nano-scale undead drivers of microbial life, biogeochemical turnover and ecosystem functions

Viruses are ubiquitous in nature and have various ecological functions. Despite their very high abundance (up to 10¹⁰ g^‑1), viruses in soil remain disregarded with just a few, mostly descriptive studies published to date. With this review we focus on the probable functioning of viruses in soil and the consequences for microbial life and turnover, related mechanisms of biogeochemical cycling of carbon (C) and nutrients, and long-term C stabilization. We draw on the limited literature for soil, the richer knowledge from aquatic ecosystems and sediments, and evidence from pure culture studies. Evidence from soil and other ecosystems indicate that the vast majority of soil bacteria are infected by phages at any time. Consequently, we introduce and adapt five concepts for the role of phages in soil: (1) Viral Shunt, (2) 'Forever Young', (3) Viral Regulatory Gate of EXOMET, (4) C sequestration by microbial necromass stabilization, and (5) Microscale divergence of C/N/P stoichiometry. The 'Viral Shunt' accounts for the short-circuiting of trophic C and nutrient transfers by virus-induced mortality. Phages (even without soil animals – the Microbial Loop concept) explain bacterial death rates and the release of easily available C and nutrients, consequently accelerating biogeochemical cycles in soil. The concept 'Forever Young' postulates that viral infection maintains the active bacterial population at a young age, because infection and lysis lead to a short life expectancy. We controversially discuss this concept in relation to hypotheses such as (1) the dormancy of most soil microorganisms, (2) maintenance energy for microorganisms, and (3) their high C use efficiency. We unify the previously suggested but unexplained concepts of 'Regulatory Gate' and 'EXOMET' through the lytic release of intracellular enzymes and metabolites. Due to the elemental composition of phages, infection results in Stoichiometric C/N/P Imbalances at the microscale, with consequences for P limitation at macroscales. The recently developed concept of 'C Sequestration by Necromass Stabilization', i.e., that C sequestered in soil derives from microbial necromass, is discussed from the new perspective of viral lysis and "entombment" of cell fragments in nano-pores. Very few studies have investigated viruses in soil, so all research directions are open, important and fascinating. The most urgent are those elucidating virus functions, their consequences for microbial life, and ecological relevance, and to confirm (or to reject) the proposed concepts. Functioning very fast at the nano-scale, the undead drivers govern microbial life in soil and biogeochemical turnover from micro to ecosystem scales.