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

Abstract

Background Viruses impact nearly all organisms on Earth, including microbial communities and their associated biogeochemical processes. In soils, highly diverse viral communities have been identified, with a global distribution seemingly driven by multiple biotic and abiotic factors, especially soil temperature and moisture. However, our current understanding of the stability of soil viral communities across time and their response to strong seasonal changes in environmental parameters remains limited. Here, we investigated the diversity and activity of environmental soil DNA and RNA viruses, focusing especially on bacteriophages, across dynamics’ seasonal changes in a snow-dominated mountainous watershed by examining paired metagenomes and metatranscriptomes. Results We identified a large number of DNA and RNA viruses taxonomically divergent from existing environmental viruses, including a significant proportion of fungal RNA viruses, and a large and unsuspected diversity of positive single-stranded RNA phages (Leviviricetes), highlighting the under-characterization of the global soil virosphere. Among these, we were able to distinguish subsets of active DNA and RNA phages that changed across seasons, consistent with a “seed-bank” viral community structure in which new phage activity, for example, replication and host lysis, is sequentially triggered by changes in environmental conditions. At the population level, we further identified virus-host dynamics matching two existing ecological models: “Kill-The-Winner” which proposes that lytic phages are actively infecting abundant bacteria, and “Piggyback-The-Persistent” which argues that when the host is growing slowly, it is more beneficial to remain in a dormant state. The former was associated with summer months of high and rapid microbial activity, and the latter with winter months of limited and slow host growth. Conclusion Taken together, these results suggest that the high diversity of viruses in soils is likely associated with a broad range of host interaction types each adapted to specific host ecological strategies and environmental conditions. As our understanding of how environmental and host factors drive viral activity in soil ecosystems progresses, integrating these viral impacts in complex natural microbiome models will be key to accurately predict ecosystem biogeochemistry.

Temporal turnover of viral biodiversity and functional potential in intertidal wetlands

“…Here, the recovered intertidal viruses were observed to infect almost all microbial lineages. Previous work has demonstrated that the variations of virus–host relationships across space and through time may reflect the degree of responses to environmental factors 32 – 34 . Consistent with these findings, the VHRs of different host lineages in intertidal zones were associated with multiple environmental factors, especially temperature, suggesting that seasonal changes were important in driving virus–host relationships.…”

Consensus statement from the first RdRp Summit: advancing RNA virus discovery at scale across communities

“…Deep sequencing of small RNAs (sRNAs) can also be advantageous to plant and mycovirus discovery, by using various sRNA size profiles depending on the organism for RNA genome assembly (35)(36)(37)(38)(39)(40). On the other hand, untargeted total RNA extraction followed by RNA-seq better reflects the global sample complexity, including host and viral diversity, and can assist with host association, further answering ecological questions (41). However, the choice of the kit used for RNA extraction can substantially influence the downstream analysis (42).…”

The role of rhizosphere phages in soil health

“…Moreover, rhizosphere phage communities vary between different plant species, due to differences in plant root exudate composition (Zhalnina et al 2018 ), which can determine the composition and abundances of plant-associated bacterial microbiomes (Wang et al 2022 ). In addition to spatial variation, the diversity and activity of phages can show dynamic temporal changes, driven by seasonal fluctuations in temperature (Coclet et al 2023 ), soil moisture (Santos-Medellin et al 2023 ), plant growth and development (Yang et al 2023 ), and anthropogenic factors such as crop management (Muscatt et al 2022 ). These external factors can also influence the intrinsic dynamics between phages and their host, e.g.…”