RNA Phages: Under-Estimated Players in Soil Ecosystems?
Clement Coclet1,2, Maureen Berg1, Roniya Thapa Magar2, Shi Wang2, Patrick O. Sorensen2, Ulas Karaoz2, Vivek Mutalik2, Eoin L. Brodie2,3, Emiley A. Eloe-Fadrosh1,2, and Simon Roux1,2* (firstname.lastname@example.org)
1DOE Joint Genome Institute; 2, Lawrence Berkeley National Laboratory; and 3University of California–Berkeley
The overarching goals of this project are to establish an analytical and experimental framework for comprehensive characterization of viral-driven alteration of microbial metabolisms in soil. The specific results presented here focus on the unexpected diversity of RNA phages detected in soil microbiomes, reveal their specific activity patterns and likely impact on bacterial lysis rate in a model soil ecosystem, and highlight several potential avenues to further characterize these soil RNA phages and their impact on microbiome processes.
Bacteriophages are now recognized as key regulators of microbial communities and processes in virtually all ecosystems, from the human gut to the global oceans. The overwhelming majority of phages described and studied so far, either via cultivation or metagenomics approaches, are double-stranded DNA phages with head-tail virion morphology, i.e., “tailed phages” from the Caudoviricetes class. In contrast, RNA-based bacteriophages are rarely reported or isolated and are typically not considered as important components of environmental microbiomes.
Here, the team combined large-scale data mining and time-series analyses to highlight the unsuspected diversity and potential ecological importance of RNA phages in soils. As part of a global survey of RNA viruses across more than 3,500 metatranscriptomes, researchers identified more than 80,000 potential RNA phages, primarily related to the known leviviruses but also including at least eight proposed new families and genera across several phyla (Neri et al. 2022). This global survey also identified a clear enrichment for leviviruses in wastewater, soil, and rhizosphere samples, suggesting these ecosystems are the primary reservoirs of novel RNA phage diversity. Through the specific analysis of a multiomics time series from East River (Colorado) watershed soils, researchers now demonstrate that RNA phage populations in these soils are highly diverse and follow similar activity levels and patterns as dsDNA phages. In particular, team members have observed an increase in RNA phage activity throughout the plant growing season, concomitant with an expected increase in microbial activity. Given the absence of known and predicted lysogenic cycles for RNA phages, they may contribute substantially to the overall bacterial cell lysis and nutrient cycling in the East River watershed, although their exact host range and infection dynamics remains to be characterized. Finally, based on these new RNA phages genomes, researchers identified novel protein families potentially associated with alternative mechanisms for host cell attachment and lysis. Ongoing computational and experimental characterization of these new attachment and lysis proteins should provide further insights in the potential host range of these RNA phages, and possibly reveal new molecules of biotechnological interests such as new single-gene lysis proteins.
Taken together with other recent surveys and studies (Callanan, et al. 2018), these results suggest that RNA phages should be more broadly considered and included in viral ecology studies, especially in soils; and they represent promising sources of novel genes and molecules for biotechnological applications.
Neri, U., et al. 2022. “Expansion of the Global RNA Virome Reveals Diverse Clades of Bacteriophages,” Cell 185, 4023–37, e18. DOI:10.1016/j.cell.2022.08.023.
Callanan, J., et al. 2018. “RNA Phage Biology in a Metagenomic Era,” Viruses 10, 386. DOI:10.3390/v10070386.
This work was supported by the U.S. Department of Energy, Office of Science, Biological and Environmental Research, Early Career Research Program awarded under UC-DOE Prime Contract DE-AC02-05CH11231. The work conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. This work was supported in part by the Laboratory Directed Research and Development Program of Lawrence Berkeley National Laboratory under U.S. Department of Energy Contract No. DE-AC02-05CH11231. A portion of this research was performed under the Facilities Integrating Collaborations for User Science (FICUS) program and used resources at the DOE Joint Genome Institute and the Environmental Molecular Sciences Laboratory (grid.436923.9), which are DOE Office of Science user facilities. Both facilities are sponsored by the Biological and Environmental Research program and operated under Contract Nos. DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). This material is based upon work supported as part of the Watershed Function science focus area funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number DE-AC02-05CH11231.