Viral lysing can alleviate microbial nutrient limitations and accumulate recalcitrant dissolved organic matter components in soil

Abstract

Viruses are critical for regulating microbial communities and biogeochemical processes affecting carbon/nutrient cycling. However, the role of soil phages in controlling microbial physiological traits and intrinsic dissolved organic matter (DOM) properties remains largely unknown. Herein, microcosm experiments with different soil phage concentrates (including no-added phages, inactive phages, and three dilutions of active phages) at two temperatures (15 °C and 25 °C) were conducted to disclose the nutrient and DOM dynamics associated with viral lysing. Results demonstrated three different phases of viral impacts on CO2 emission at both temperatures, and phages played a role in maintaining Q10 within bounds. At both temperatures, microbial nutrient limitations (especially P limitation) were alleviated by viral lysing as determined by extracellular enzyme activity (decreased Vangle with active phages). Additionally, the re-utilization of lysate-derived DOM by surviving microbes stimulated an increase of microbial metabolic efficiency and recalcitrant DOM components (e.g., SUV254, SUV260 and HIX). This research provides direct experimental evidence that the “viral shuttle” exists in soils, whereby soil phages increase recalcitrant DOM components. Our findings advance the understanding of viral controls on soil biogeochemical processes, and provide a new perspective for assessing whether soil phages provide a net “carbon sink” vs. “carbon source” in soils.

Virus diversity and activity is driven by snowmelt and host dynamics in a high-altitude watershed soil ecosystem

“…These results suggest that RNA viruses are an integral component of global soil ecosystems, with a diversity and activity driven by the growth of their hosts and the environmental parameters which affect them [107]. The detection of expressed genes related to lysis functions, combined with an increase in this activity from Spring to Summer, suggests that viral lysis may influence the global availability of nutrients and organic matter in the ERW soils, as recently shown in microcosm experiments [108], especially in periods of high microbial activity and growth. Meanwhile, for other vOTUs, the specific expression of genes not involved in genome replication, capsid formation, or lysis would be consistent with an active reprogramming of their host metabolism outside of (or prior to) active virion production.…”

Soil viruses reduce greenhouse gas emissions and promote microbial necromass accrual

“…The higher microbial abundance and necromass content in the soils of virus treatment indicate that microbial community turnover was accelerated under viral predation. Viral lysate-derived dissolved organic C and other labile nutrients can increase microbial metabolic efficiency and promote microbial biomass synthesis (Zhao et al, 2019; Tong et al, 2023). Accelerated microbial turnover can positively influence the contribution of microbial necromass C and N to SOC and N storage (Hagerty et al, 2014; Prommer et al, 2020).…”

Meeting Report of the Second Symposium of the Belgian Society for Viruses of Microbes and Launch of the Phage Valley

“…The second speaker, Ella Sieradzki from the “Ecole Centrale de Lyon”, described phage dynamics in soil ecosystems [ 7 , 8 ]. Using isotope incorporation into viral and microbial DNA, phage–host temporal dynamics were characterized, revealing taxon-specific trends in viral–host dynamics.…”