Ecological and evolutionary patterns of virus-host interactions throughout a grassland soil depth profile

Abstract

Background:Soil microbes play pivotal roles in global carbon cycling, however the fundamental interactions between microbes and their infecting viruses remain unclear. This is exacerbated with soil depth, where the patterns of viral dispersal, ecology, and evolution are markedly underexplored. To investigate viral communities across soil depth, we leveraged a publicly available metagenomic data set sampled from grassland soil in northern California.Results:10,196 non-redundant vOTUs were recovered from soil sampled from 20 cm to 120 cm below the surface. Viral prevalence was high throughout the soil depth profile, with viruses infecting dominant soil phyla, includingActinomycetota. Contrary to leading hypotheses, lysogeny did not dominate in the soil viral communities. Viral diversity was investigated at both the population-level (i.e., macro diversity) and strain-level (i.e., micro diversity) to reveal diverse ecological and evolutionary patterns of virus-host interactions in surface and subsurface soil.Conclusions:By investigating viral micro diversity in soil for the first time, we have uncovered patterns of antagonistic co-evolution across both surface and subsurface soils. Furthermore, we have provided evidence of soil viruses augmenting the remineralisation of soil carbon. While we continue to yield a more comprehensive understanding of soil viral ecology, our work appeals to future researchers to continue to investigate subsurface viral communities.

Benchmarking Bioinformatic Virus Identification Tools Using Real-World Metagenomic Data across Biomes

“…The soil datasets also had the lowest percentage of homologous contigs between the viral and microbial datasets. As overlapping viral and microbial sequences might represent active and integrated temperate viruses, respectively, we hypothesize that there might be more lytic viruses in soil than in seawater and gut, in line with previous findings that lysogeny genes are scarce in soil viromes 11,[79][80][81][82] . These overlapping sequences were removed from our benchmarking analysis.…”

Viral but not bacterial community succession is characterized by extreme turnover shortly after rewetting dry soils

“…Thus far, lysogeny genes seem to be at low abundance in soil viromes 18,[70][71][72] , including in this study. However, results here also suggest that viral particle (virion) survival in dry soils is relatively rare (for example, two of our soils had dry soil virion abundances below detection limits), such that sustaining the extreme bloom of viral diversity upon wet-up from pre-existing virions alone would seem to require numerous successful infections sparked by few individuals spread across a highly diverse soil virosphere.…”

“…For each of the four soil types, dry soils were added to highly replicated microcosms and rewetted to ~25% soil moisture content with sterile water (Supplementary Figure 1c). Microcosms were destructively sampled at seven time points over ten days: T0 (dry) and T1-T6 (24,48,72,120,168, and 240 hours post-wet-up, respectively), and a control set of unwetted soil microcosms was also sampled after 10 days (Figure 1b). To characterize the short-term temporal dynamics of the soil viral community response to rewetting, as well as compare temporal patterns in bacterial and viral communities and relic DNA following wet-up, we generated 144 viromes (84 DNase-treated and 60 untreated) and 84 total metagenomes (Figure 1c).…”

Viruses in deep-sea cold seep sediments harbor diverse survival mechanisms and remain genetically conserved within species

“…Intra-population genetic variations (i.e., microdiversity) can also improve virus adaptation to their environment by driving phenotypic variation 21, 22 . For example, depth-dependent evolutionary strategies of viruses were observed in the Mediterranean Sea 9 and grassland soil in northern California 10 . Large viral microdiversity was observed for perhaps the most abundant ocean virus in temperate and tropical waters infecting Pelagibacter 23 , whereas viruses were under significantly low evolutionary pressures in stable subzero Arctic brines 24 .…”

“…As foreign mobile genetic elements, viruses face a wide repertoire of antiviral defense systems, including restriction-modification (RM) and CRISPR-Cas 8 . In line with antagonistic co-evolution of viruses and their hosts 9, 10 , viruses have developed efficient and robust counter-defense systems, such as anti-restriction, anti-CRISPR and other counter-defense proteins 11, 12 . Diversity-generating retroelements (DGRs) containing reverse transcriptase (RT) are another important diversification mechanism for driving sustained amino acid-level diversification of their target domains 13, 14 .…”