Abstract
ABSTRACTDuring the last several decades, viruses have been increasingly recognized for their abundance, ubiquity, and important roles in different ecosystems. Despite known contributions to aquatic systems, few studies examine viral abundance and community structure over time in terrestrial ecosystems. The effects of land conversion and land management on soil microbes have been previously investigated, but their effects on virus population are not well studied. This study examined annual dynamics of viral abundance in soils from a native tallgrass prairie and two croplands, conventional till winter wheat and no-till canola, in Oklahoma. Virus-like particle (VLP) abundance varied across sites, and showed clear seasonal shifts. VLP abundance significantly correlated with environmental variables that were generally reflective of land use, including air temperature, soil nitrogen, and plant canopy coverage. Structural equation modeling supported the effects of land use on soil communities by emphasizing interactions between management, environmental factors, and viral and bacterial abundance. Between the viral metagenomes from the prairie and tilled wheat field, 1,231 unique viral operational taxonomic units (vOTUs) were identified, and only five were shared that were rare in the contrasting field. Only 13% of the vOTUs had similarity to previously identified viruses in the RefSeq database, with only 7% having known taxonomic classification. Together, our findings indicated land use and tillage practices influence virus abundance and community structure. Analyses of viromes over time and space are vital to viral ecology in providing insight on viral communities and key information on interactions between viruses, their microbial hosts, and the environment.IMPORTANCE Conversion of land alters the physiochemical and biological environments by not only changing the aboveground community, but also modifying the soil environment for viruses and microbes. Soil microbial communities are critical to nutrient cycling, carbon mineralization, and soil quality; and viruses are known for influencing microbial abundance, community structure, and evolution. Therefore, viruses are considered an important part of soil functions in terrestrial ecosystems. In aquatic environments, virus abundance generally exceeds bacterial counts by an order of magnitude, and they are thought to be one of the greatest genetic reservoirs on the planet. However, data are extremely limited on viruses in soils, and even less is known about their responses to the disturbances associated with land use and management. The study provides important insights into the temporal dynamics of viral abundance and the structure of viral communities in response to the common practice of turning native habitats into arable soils.
Highlights
Viruses have been making their way to the forefront of ecological research for their significant roles in marine and terrestrial ecosystems, being found everywhere that life exists
With advances toward optimized methods for studying terrestrial viruses, recent studies in a thawing permafrost gradient recovered roughly 2,000 viruses approximately doubling the number of known genera in the RefSeq database at the time [35, 36] with the number of uncultivated virus genomes greatly surpassing the number of sequenced virus isolates in publicly available databases [37]. Such studies demonstrate that metagenomic analysis of a single environmental gradient has the ability to greatly expand the knowledge of terrestrial viruses. It emphasizes the importance of including viral abundance and viral community structure in studies to fully understand the dynamics of soil ecosystems in response to environmental changes
Our results indicated that soil properties, plant canopy cover, and environmental factors such as air temperature, most of which are further controlled by land use and land management practices, are important in shaping virus-host interactions, along with virus and host abundance
Summary
Viruses have been making their way to the forefront of ecological research for their significant roles in marine and terrestrial ecosystems, being found everywhere that life exists. Converting previously natural land into arable soils results in above and below ground species loss, allowing species invasion, as well as introducing disturbances to soil and biological processes [15,16,17] Together, these anthropogenic activities act as environmental stressors greatly impacting soil ecosystems with little known about the effects on virus populations. While studies in marine environments have presented clear temporal dynamics in viral abundance and community structure [27, 28], limited research leaves much to be discovered about the spatiotemporal changes of viruses in soils of terrestrial ecosystems. Such studies demonstrate that metagenomic analysis of a single environmental gradient has the ability to greatly expand the knowledge of terrestrial viruses It emphasizes the importance of including viral abundance and viral community structure in studies to fully understand the dynamics of soil ecosystems in response to environmental changes
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