Unraveling Spatiotemporal and Physicochemical Constraints on Soil Viral Community Composition and Viral Particle Integrity
Anneliek M. ter Horst, Christian Santos-Medellín, Sara E. Geonczy, Jane D. Fudyma, and Joanne B. Emerson* (email@example.com)
University of California–Davis
The overarching goal of this project is to assess and compare the contributions of active, infectious viruses and inert viral particles to biogeochemistry across diverse terrestrial ecosystems. Using a multiomics approach, the team seeks to establish spatiotemporal patterns in soil viral community composition and activity linked to host carbon and nitrogen metabolism in grasslands, shrublands, woodlands, and wetlands. Leveraging a prescribed forest fire and a peatland temperature and atmospheric CO2 manipulation experiment also allows exploration into feedbacks between soil viruses and carbon dynamics in response to environmental change. Through laboratory experiments, researchers are investigating the chemical composition, fate, transport, and integrity of viral particles in soil. By integrating field and laboratory experiments across a variety of soil edaphic properties and spatiotemporal scales, this project is expanding understanding of the soil virosphere and its influence on carbon and nutrient cycling.
Viruses have been recognized as highly abundant but poorly characterized members of the soil microbiome. By infecting soil microbes, viruses likely have substantial impacts on terrestrial biogeochemical processes under their hosts’ control. Viral particles (virions) may also play more direct roles in soil biogeochemical cycling as packets of carbon, nitrogen, and phosphorus, but the time scales and environmental conditions that determine virion infectivity, transport, and/or sorption to soil particles are unknown. This project uses a combination of field, laboratory, and computational approaches to distinguish between infective and inert virions and to assess their respective contributions to soil biogeochemical cycling.
Using a post-0.22 µm ‘viral size-fraction’ metagenomics (viromics) approach, researchers are exploring the conditions and temporal scales over which virions are produced, remain infective, and decay in soil. Research has shown that viromes can recover ~500 times more viral sequence than total metagenomes, but at the start of this project, it was unknown whether viromes reflected recent or long past infections. Results suggest that soil viromes generally capture very recently active viral communities, particularly in moist soil, but can reflect earlier infections in less active communities (e.g., in seasonally dry soils) and can be dominated by compromised (inert) viral particles after extreme temperature perturbations (e.g., heating to 90ºC or freezing).
The project’s interpretation that most soil viromes capture a short window of recent activity is consistent with repeated findings of highly divergent soil viral communities over spatial distances as short as 1 m in nearly all habitats explored thus far. Results from the first 2 years of this award suggested that soil viral communities were so distinct by site on a regional scale that more localized habitat comparisons would be more tractable (Durham et al. 2022). Seven distinct wetland habitats (sites) were thus sampled over a 0.6 km2 area in the Bodega Bay Natural Reserve on the California Pacific Coast. Viral communities were most distinct by site, with few populations shared between sites. Secondarily, viral communities with similar habitat characteristics (e.g., plant community composition and/or salinity) were most similar. Although reducing the spatial area of the study and selecting seemingly similar habitats (all wetlands) improved resolution of viral ecological patterns, ongoing efforts are focused on further reducing complexity.
Centered on a highly spatiotemporally resolved viromic study of two habitats in the Jepson Prairie grassland (eight locations, 30 time points since November 2020), ongoing work seeks to unravel the relative contributions of space, time, habitat, and dispersal on patterns of soil viral community composition. Briefly, viromes at Jepson Prairie were most distinct by habitat (between mounds and their adjacent swales, defined by differences in topography, plant community composition, and hydrology), but viral community compositional patterns over time were different within each habitat. The four swales exhibited similar viral community successional patterns over time, likely reflecting greater mixing in the swale habitats via intermittent flooding, whereas the four mounds (which rise ~0.5 m above swales and never flood) were more distinct over space, reflecting dispersal limitation. Analysis of the full dataset of >300 viromes is ongoing.
To investigate physicochemical constraints on virion integrity and viral community composition, researchers are analyzing data from three burned habitats and a laboratory temperature manipulation experiment. In shrublands and woodlands that burned during the dry season in the LNU Complex Fires in August 2020, the team is characterizing viral community successional dynamics after fire. A prescribed burn in a mixed conifer forest in Spring 2021 was also leveraged to compare burned and unburned soil viral communities. Preliminary results suggest that habitat and location differentiate viral community composition more than the impact of fire, but viral richness was lower post-fire than in unburned or pre-fire soils. The degree of virion inactivation and the timing of viral community recovery post-fire seem to depend on soil moisture and depth. Briefly, heating experiments are revealing that viral particle ‘survival’ thresholds are similar to those known for bacteria, with a reduction in survival at 60ºC and nearly complete removal of intact virions (with some inert, compromised virions remaining) at 90ºC.
Together, these results are revealing that the relative importance of spatial distance (and dispersal), time, and environmental conditions in structuring viral communities varies. With substantial differences in environmental parameters, habitat seems to trump all other factors at both local and global scales, but in local environments under similar conditions, space and time can be important. Results from this project are facilitating a better understanding of viral contributions to terrestrial biogeochemical cycling, both as dynamic components of soil organic matter and through their infection of hosts responsible for carbon and nutrient cycling.
Durham, D. M., et al. 2022. “Substantial Differences in Soil Viral Community Composition Within and Among Four Northern California Habitats,” ISME Communications 2, 100.
This research was supported by the U.S. Department of Energy’s (DOE) Biological and Environmental Research (BER) Program under grant no. DE-SC0021198.