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Soil viral diversity, ecology and climate change – Nature.com

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Nature Reviews Microbiology (2022)
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Soil viruses are highly abundant and have important roles in the regulation of host dynamics and soil ecology. Climate change is resulting in unprecedented changes to soil ecosystems and the life forms that reside there, including viruses. In this Review, we explore our current understanding of soil viral diversity and ecology, and we discuss how climate change (such as extended and extreme drought events or more flooding and altered precipitation patterns) is influencing soil viruses. Finally, we provide our perspective on future research needs to better understand how climate change will impact soil viral ecology.
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Helsley, K. R., Brown, T. M., Furlong, K. & Williamson, K. E. Applications and limitations of tea extract as a virucidal agent to assess the role of phage predation in soils. Biol. Fertil. Soils 50, 263–274 (2014).
Article  Google Scholar 
Suttle, C. A. Marine viruses — major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801–812 (2007).
Article  CAS  PubMed  Google Scholar 
Winter, C., Bouvier, T., Weinbauer, M. G. & Thingstad, T. F. Trade-offs between competition and defense specialists among unicellular planktonic organisms: the “killing the winner” hypothesis revisited. Microbiol. Mol. Biol. Rev. 74, 42–57 (2010).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Pratama, A. A. & van Elsas, J. D. The ‘neglected’ soil virome–potential role and impact. Trends Microbiol. 26, 649–662 (2018).
Article  CAS  PubMed  Google Scholar 
Williamson, K. E., Fuhrmann, J. J., Wommack, K. E. & Radosevich, M. Viruses in soil ecosystems: an unknown quantity within an unexplored territory. Annu. Rev. Virol. 4, 201–219 (2017).
Article  CAS  PubMed  Google Scholar 
Gonzalez-Martin, C., Teigell-Perez, N., Lyles, M., Valladares, B. & Griffin, D. W. Epifluorescent direct counts of bacteria and viruses from topsoil of various desert dust storm regions. Res. Microbiol. 164, 17–21 (2013).
Article  PubMed  Google Scholar 
Ashelford, K. E., Day, M. J. & Fry, J. C. Elevated abundance of bacteriophage infecting bacteria in soil. Appl. Environ. Microbiol. 69, 285–289 (2003).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Bowatte, S., Newton, P. C., Takahashi, R. & Kimura, M. High frequency of virus-infected bacterial cells in a sheep grazed pasture soil in New Zealand. Soil Biol. Biochem. 42, 708–712 (2010).
Article  CAS  Google Scholar 
Takahashi, R. et al. High frequency of phage-infected bacterial cells in a rice field soil in Japan. Soil Sci. Plant Nutr. 57, 35–39 (2011).
Article  Google Scholar 
Williamson, K. E., Radosevich, M. & Wommack, K. E. Abundance and diversity of viruses in six Delaware soils. Appl. Environ. Microbiol. 71, 3119–3125 (2005).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Liang, X. et al. Lysogenic reproductive strategies of viral communities vary with soil depth and are correlated with bacterial diversity. Soil Biol. Biochem. 144, 107767 (2020).
Article  CAS  Google Scholar 
Emerson, J. B. et al. Host-linked soil viral ecology along a permafrost thaw gradient. Nat. Microbiol. 3, 870–880 (2018).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Jansson, J. K. & Hofmockel, K. S. Soil microbiomes and climate change. Nat. Rev. Microbiol. 18, 35–46 (2020).
Article  CAS  PubMed  Google Scholar 
Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl Acad. Sci. USA 103, 626–631 (2006).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Bi, L. et al. Diversity and potential biogeochemical impacts of viruses in bulk and rhizosphere soils. Environ. Microbiol. 23, 588–599 (2021).
Article  CAS  PubMed  Google Scholar 
Starr, E. P., Nuccio, E. E., Pett-Ridge, J., Banfield, J. F. & Firestone, M. K. Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil. Proc. Natl Acad. Sci. USA 116, 25900–25908 (2019).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Hurst, C. J., Gerba, C. P. & Cech, I. Effects of environmental variables and soil characteristics on virus survival in soil. Appl. Environ. Microbiol. 40, 1067–1079 (1980).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Williamson, K. E., Wommack, K. E. & Radosevich, M. Sampling natural viral communities from soil for culture-independent analyses. Appl. Environ. Microbiol. 69, 6628–6633 (2003).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Wu, R. et al. DNA viral diversity, abundance, and functional potential vary across grassland soils with a range of historical moisture regimes. mBio 12, e02595521 (2021).
Article  Google Scholar 
Chen, L. et al. Effect of different long-term fertilization regimes on the viral community in an agricultural soil of southern China. Eur. J. Soil Biol. 62, 121–126 (2014).
Article  Google Scholar 
Williamson, K. E., Radosevich, M., Smith, D. W. & Wommack, K. E. Incidence of lysogeny within temperate and extreme soil environments. Environ. Microbiol. 9, 2563–2574 (2007).
Article  CAS  PubMed  Google Scholar 
Narr, A., Nawaz, A., Wick, L. Y., Harms, H. & Chatzinotas, A. Soil viral communities vary temporally and along a land use transect as revealed by virus-like particle counting and a modified community fingerprinting approach (fRAPD). Front. Microbiol. 8, 1975 (2017).
Article  PubMed  PubMed Central  Google Scholar 
Fierer, N. et al. Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl. Environ. Microbiol. 73, 7059–7066 (2007).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Paez-Espino, D. et al. Uncovering Earth’s virome. Nature 536, 425–430 (2016).
Article  CAS  PubMed  Google Scholar 
Santos-Medellin, C. et al. Viromes outperform total metagenomes in revealing the spatiotemporal patterns of agricultural soil viral communities. ISME J. 15, 1956–1970 (2021).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Roux, S. et al. IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses. Nucleic Acids Res. 49, D764–D775 (2021).
Article  CAS  PubMed  Google Scholar 
Brum, J. R. & Sullivan, M. B. Rising to the challenge: accelerated pace of discovery transforms marine virology. Nat. Rev. Microbiol. 13, 147–159 (2015).
Article  CAS  PubMed  Google Scholar 
Coutinho, F. H., Gregoracci, G. B., Walter, J. M., Thompson, C. C. & Thompson, F. L. Metagenomics sheds light on the ecology of marine microbes and their viruses. Trends Microbiol. 26, 955–965 (2018).
Article  CAS  PubMed  Google Scholar 
Guo, J. et al. VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome 9, 1–13 (2021).
Article  Google Scholar 
Ren, J., Ahlgren, N. A., Lu, Y. Y., Fuhrman, J. A. & Sun, F. VirFinder: a novel k-mer based tool for identifying viral sequences from assembled metagenomic data. Microbiome 5, 1–20 (2017).
Article  Google Scholar 
Shaffer, M. et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 48, 8883–8900 (2020).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Kieft, K., Zhou, Z. & Anantharaman, K. VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences. Microbiome 8, 1–23 (2020).
Article  Google Scholar 
Paez-Espino, D., Pavlopoulos, G. A., Ivanova, N. N. & Kyrpides, N. C. Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data. Nat. Protoc. 12, 1673–1682 (2017).
Article  CAS  PubMed  Google Scholar 
Swanson, M. et al. Viruses in soils: morphological diversity and abundance in the rhizosphere. Ann. Appl. Biol. 155, 51–60 (2009).
Article  Google Scholar 
Wu, R. et al. Moisture modulates soil reservoirs of active DNA and RNA viruses. Commun. Biol. 4, 1–11 (2021).
Article  Google Scholar 
Trubl, G. et al. Soil viruses are underexplored players in ecosystem carbon processing. mSystems 3, e00076-18 (2018).
Article  PubMed  PubMed Central  Google Scholar 
Al-Shayeb, B. et al. Clades of huge phages from across Earth’s ecosystems. Nature 578, 425–431 (2020).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Fischer, M. G. Giant viruses come of age. Curr. Opin. Microbiol. 31, 50–57 (2016).
Article  PubMed  Google Scholar 
Raoult, D. et al. The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344–1350 (2004).
Article  CAS  PubMed  Google Scholar 
Pagnier, I. et al. A decade of improvements in Mimiviridae and Marseilleviridae isolation from amoeba. Intervirology 56, 354–363 (2013).
Article  PubMed  Google Scholar 
Boughalmi, M. et al. High‐throughput isolation of giant viruses of the Mimiviridae and Marseilleviridae families in the Tunisian environment. Environ. Microbiol. 15, 2000–2007 (2013).
Article  PubMed  Google Scholar 
Legendre, M. et al. Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc. Natl Acad. Sci. USA 111, 4274–4279 (2014).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Legendre, M. et al. In-depth study of Mollivirus sibericum, a new 30,000-y-old giant virus infecting Acanthamoeba. Proc. Natl Acad. Sci. USA 112, E5327–E5335 (2015).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Yoosuf, N. et al. Draft genome sequences of Terra1 and Terra2 viruses, new members of the family Mimiviridae isolated from soil. Virology 452, 125–132 (2014).
Article  PubMed  Google Scholar 
Schulz, F. et al. Hidden diversity of soil giant viruses. Nat. Commun. 9, 4881 (2018).
Article  PubMed  PubMed Central  Google Scholar 
Schulz, F. et al. Giant virus diversity and host interactions through global metagenomics. Nature 578, 432–436 (2020).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Hulo, C. et al. ViralZone: a knowledge resource to understand virus diversity. Nucleic Acids Res. 39, D576–D582 (2011).
Article  CAS  PubMed  Google Scholar 
Adriaenssens, E. M. et al. Environmental drivers of viral community composition in Antarctic soils identified by viromics. Microbiome 5, 1–14 (2017).
Article  Google Scholar 
Liang, X. et al. Viral abundance and diversity vary with depth in a southeastern United States agricultural ultisol. Soil Biol. Biochem. 137, 107546 (2019).
Article  CAS  Google Scholar 
International Committee on Taxonomy of Viruses Executive Committee. The new scope of virus taxonomy: partitioning the virosphere into 15 hierarchical ranks. Nat. Microbiol. 5, 668–674 (2020).
Article  CAS  Google Scholar 
Adriaenssens, E. M. et al. Taxonomy of prokaryotic viruses: 2018-2019 update from the ICTV bacterial and archaeal viruses subcommittee. Arch. Virol. 165, 1253–1260 (2020).
Article  CAS  PubMed  Google Scholar 
Roux, S. et al. Minimum information about an uncultivated virus genome (MIUViG). Nat. Biotechnol. 37, 29–37 (2019).
Article  CAS  PubMed  Google Scholar 
Kim, K.-H. et al. Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl. Environ. Microbiol. 74, 5975–5985 (2008).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Han, L.-L., Yu, D.-T., Zhang, L.-M., Shen, J.-P. & He, J.-Z. Genetic and functional diversity of ubiquitous DNA viruses in selected Chinese agricultural soils. Sci. Rep. 7, 1–10 (2017).
Google Scholar 
Reavy, B. et al. Distinct circular single-stranded DNA viruses exist in different soil types. Appl. Environ. Microbiol. 81, 3934–3945 (2015).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Trubl, G. et al. Towards optimized viral metagenomes for double-stranded and single-stranded DNA viruses from challenging soils. PeerJ 7, e7265 (2019).
Article  PubMed  PubMed Central  Google Scholar 
Marine, R. et al. Caught in the middle with multiple displacement amplification: the myth of pooling for avoiding multiple displacement amplification bias in a metagenome. Microbiome 2, 3 (2014).
Article  PubMed  PubMed Central  Google Scholar 
Han, L.-L. et al. Distribution of soil viruses across China and their potential role in phosphorous metabolism. Environ. Microbiome 17, 6 (2022).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Peck, K. M. & Lauring, A. S. Complexities of viral mutation rates. J. Virol. 92, e01031-17 (2018).
Article  PubMed  PubMed Central  Google Scholar 
Malathi, V. & Renuka Devi, P. ssDNA viruses: key players in global virome. Virusdisease 30, 3–12 (2019).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Steward, G. F. et al. Are we missing half of the viruses in the ocean? ISME J. 7, 672–679 (2013).
Article  CAS  PubMed  Google Scholar 
Hillary, L. S., Adriaenssens, E. M., Jones, D. L. & McDonald, J. E. RNA-viromics reveals diverse communities of soil RNA viruses with the potential to affect grassland ecosystems across multiple trophic levels. ISME Commun. 2, 1–10 (2022).
Article  Google Scholar 
Schroeder, J. W., Dobson, A., Mangan, S. A., Petticord, D. F. & Herre, E. A. Mutualist and pathogen traits interact to affect plant community structure in a spatially explicit model. Nat. Commun. 11, 1–10 (2020).
Google Scholar 
Chen, I.-M. A. et al. The IMG/M data management and analysis system v. 6.0: new tools and advanced capabilities. Nucleic Acids Res. 49, D751–D763 (2021).
Article  CAS  PubMed  Google Scholar 
Neri, U. et al. A five-fold expansion of the global RNA virome reveals multiple new clades of RNA bacteriophages. Zenodo https://doi.org/10.5281/zenodo.6553771 (2022).
Article  Google Scholar 
Koonin, E. V. et al. Global organization and proposed megataxonomy of the virus world. Microbiol. Mol. Biol. Rev. 84, e00061-19 (2020).
Article  PubMed  PubMed Central  Google Scholar 
Neri, U. et al. A five-fold expansion of the global RNA virome reveals multiple new clades of RNA bacteriophages. Preprint at bioRxiv https://doi.org/10.1101/2022.02.15.480533 (2022).
Article  Google Scholar 
Albright, M. B. et al. Experimental evidence for the impact of soil viruses on carbon cycling during surface plant litter decomposition. ISME Commun. 2, 24 (2022).
Article  Google Scholar 
Braga, L. P. et al. Impact of phages on soil bacterial communities and nitrogen availability under different assembly scenarios. Microbiome 8, 52 (2020).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Wang, Y. et al. Heterogeneity of soil bacterial and bacteriophage communities in three rice agroecosystems and potential impacts of bacteriophage on nutrient cycling. Environ. Microbiome 17, 17 (2022).
Article  PubMed  PubMed Central  Google Scholar 
Williamson, K. E., Schnitker, J. B., Radosevich, M., Smith, D. W. & Wommack, K. E. Cultivation-based assessment of lysogeny among soil bacteria. Microb. Ecol. 56, 437–447 (2008).
Article  PubMed  Google Scholar 
Huang, D. et al. Enhanced mutualistic symbiosis between soil phages and bacteria with elevated chromium-induced environmental stress. Microbiome 9, 150 (2021).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Ghosh, D. et al. Acyl-homoserine lactones can induce virus production in lysogenic bacteria: an alternative paradigm for prophage induction. Appl. Environ. Microbiol. 75, 7142–7152 (2009).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Silveira, C. B. & Rohwer, F. L. Piggyback-the-winner in host-associated microbial communities. NPJ Biofilms Microbiomes 2, 16010 (2016).
Article  PubMed  PubMed Central  Google Scholar 
Knowles, B. et al. Lytic to temperate switching of viral communities. Nature 531, 466–470 (2016).
Article  CAS  PubMed  Google Scholar 
Thingstad, T. F. & Lignell, R. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13, 19–27 (1997).
Article  Google Scholar 
Thingstad, T. F. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45, 1320–1328 (2000).
Article  Google Scholar 
Stewart, F. M. & Levin, B. R. The population biology of bacterial viruses: why be temperate. Theor. Popul. Biol. 26, 93–117 (1984).
Article  CAS  PubMed  Google Scholar 
Obeng, N., Pratama, A. A. & van Elsas, J. D. The significance of mutualistic phages for bacterial ecology and evolution. Trends Microbiol. 24, 440–449 (2016).
Article  CAS  PubMed  Google Scholar 
Liang, X. & Radosevich, M. Commentary: a host-produced quorum-sensing autoinducer controls a phage lysis-lysogeny decision. Front. Microbiol. 10, 1201 (2019).
Article  PubMed  PubMed Central  Google Scholar 
Parikka, K. J., Le Romancer, M., Wauters, N. & Jacquet, S. Deciphering the virus‐to‐prokaryote ratio (VPR): insights into virus–host relationships in a variety of ecosystems. Biol. Rev. 92, 1081–1100 (2017).
Article  PubMed  Google Scholar 
Roy, K. et al. Temporal dynamics of soil virus and bacterial populations in agricultural and early plant successional soils. Front. Microbiol. 11, 1494 (2020).
Article  PubMed  PubMed Central  Google Scholar 
Dedrick, R. M. et al. Prophage-mediated defence against viral attack and viral counter-defence. Nat. Microbiol. 2, 16251 (2017).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Boyd, E. F. Bacteriophage-encoded bacterial virulence factors and phage–pathogenicity island interactions. Adv. Virus Res. 82, 91–118 (2012).
Article  CAS  PubMed  Google Scholar 
Bondy-Denomy, J. et al. Prophages mediate defense against phage infection through diverse mechanisms. ISME J. 10, 2854–2866 (2016).
Article  PubMed  PubMed Central  Google Scholar 
Schuch, R. & Fischetti, V. A. The secret life of the anthrax agent Bacillus anthracis: bacteriophage-mediated ecological adaptations. PLoS ONE 4, e6532 (2009).
Article  PubMed  PubMed Central  Google Scholar 
Koskella, B. & Brockhurst, M. A. Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol. Rev. 38, 916–931 (2014).
Article  CAS  PubMed  Google Scholar 
Levin, B. R. & Bull, J. J. Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2, 166–173 (2004).
Article  CAS  PubMed  Google Scholar 
Paterson, S. et al. Antagonistic coevolution accelerates molecular evolution. Nature 464, 275–278 (2010).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317–327 (2010).
Article  CAS  PubMed  Google Scholar 
Nuñez, J. K., Lee, A. S., Engelman, A. & Doudna, J. A. Integrase-mediated spacer acquisition during CRISPR–Cas adaptive immunity. Nature 519, 193–198 (2015).
Article  PubMed  PubMed Central  Google Scholar 
Sant, D. G., Woods, L. C., Barr, J. J. & McDonald, M. J. Host diversity slows bacteriophage adaptation by selecting generalists over specialists. Nat. Ecol. Evol. 5, 350–359 (2021).
Article  PubMed  Google Scholar 
Poisot, T., Lounnas, M. & Hochberg, M. E. The structure of natural microbial enemy-victim networks. Ecol. Process. 2, 13 (2013).
Article  Google Scholar 
Trubl, G. et al. Active virus-host interactions at sub-freezing temperatures in Arctic peat soil. Microbiome 9, 1–15 (2021).
Article  Google Scholar 
Poullain, V., Gandon, S., Brockhurst, M. A., Buckling, A. & Hochberg, M. E. The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution 62, 1–11 (2008).
PubMed  Google Scholar 
McGee, L. W. et al. Synergistic pleiotropy overrides the costs of complexity in viral adaptation. Genetics 202, 285–295 (2016).
Article  CAS  PubMed  Google Scholar 
Wommack, K. E. & Colwell, R. R. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114 (2000).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Starr, E. P. et al. Stable-isotope-informed, genome-resolved metagenomics uncovers potential cross-kingdom interactions in Rhizosphere soil. mSphere 6, e00085-21 (2021).
Article  PubMed Central  Google Scholar 
Osterhout, R. E., Figueroa, I. A., Keasling, J. D. & Arkin, A. P. Global analysis of host response to induction of a latent bacteriophage. BMC Microbiol. 7, 82 (2007).
Article  PubMed  PubMed Central  Google Scholar 
Quesada, J. M., Soriano, Ma. I. & Espinosa-Urgel, M. Stability of a Pseudomonas putida KT2440 bacteriophage-carried genomic island and its impact on rhizosphere fitness. Appl. Environ. Microbiol. 78, 6963–6974 (2012).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Li, G., Cortez, M. H., Dushoff, J. & Weitz, J. S. When to be temperate: on the fitness benefits of lysis vs. lysogeny. Virus Evol. 6, veaa042 (2020).
Article  PubMed  PubMed Central  Google Scholar 
Jin, M. et al. Diversities and potential biogeochemical impacts of mangrove soil viruses. Microbiome 7, 58 (2019).
Article  PubMed  PubMed Central  Google Scholar 
Zheng, X. et al. Organochlorine contamination enriches virus-encoded metabolism and pesticide degradation associated auxiliary genes in soil microbiomes. ISME J. 16, 1397–1408 (2022).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Wu, R. et al. Structural characterization of a soil viral auxiliary metabolic gene product–a functional chitosanase. Nat. Commun. 13, 5485 (2022).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Pedersen, J. S. T. et al. An assessment of the performance of scenarios against historical global emissions for IPCC reports. Glob. Environ. Change 66, 102199 (2021).
Article  Google Scholar 
Girardin, G. et al. Viruses carried to soil by irrigation can be aerosolized later during windy spells. Agron. Sustain. Dev. 36, 59 (2016).
Article  Google Scholar 
Chen, P.-S. et al. Ambient influenza and avian influenza virus during dust storm days and background days. Environ. Health Perspect. 118, 1211–1216 (2010).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Zablocki, O., Adriaenssens, E. M. & Cowan, D. Diversity and ecology of viruses in hyperarid desert soils. Appl. Environ. Microbiol. 82, 770–777 (2016).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Kimura, M., Jia, Z.-J., Nakayama, N. & Asakawa, S. Ecology of viruses in soils: past, present and future perspectives. Soil Sci. Plant Nutr. 54, 1–32 (2008).
Article  Google Scholar 
Yeager, J. & O’Brien, R. Enterovirus inactivation in soil. Appl. Environ. Microbiol. 38, 694–701 (1979).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Reanney, D. & Marsh, S. The ecology of viruses attacking Bacillus stearothermophilus in soil. Soil Biol. Biochem. 5, 399–408 (1973).
Article  Google Scholar 
Wu, R. et al. Targeted assemblies of cas1 suggest CRISPR-Cas’s response to soil warming. ISME J. 14, 1651–1662 (2020).
Article  PubMed  PubMed Central  Google Scholar 
Hugelius, G. et al. Estimated stocks of circumpolar permafrost carbon with quantified uncertainty ranges and identified data gaps. Biogeosciences 11, 6573–6593 (2014).
Article  Google Scholar 
Graham, D. E. et al. Microbes in thawing permafrost: the unknown variable in the climate change equation. ISME J. 6, 709–712 (2012).
Article  CAS  PubMed  Google Scholar 
Jansson, J. K. & Taş, N. The microbial ecology of permafrost. Nat. Rev. Microbiol. 12, 414–425 (2014).
Article  CAS  PubMed  Google Scholar 
Taş, N. et al. Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest. ISME J. 8, 1904–1919 (2014).
Article  PubMed  PubMed Central  Google Scholar 
Taş, N. et al. Landscape topography structures the soil microbiome in arctic polygonal tundra. Nat. Commun. 9, 777 (2018).
Article  PubMed  PubMed Central  Google Scholar 
Mackelprang, R. et al. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480, 368–371 (2011).
Article  CAS  PubMed  Google Scholar 
Mondav, R. et al. Discovery of a novel methanogen prevalent in thawing permafrost. Nat. Commun. 5, 3212 (2014).
Article  PubMed  Google Scholar 
Rivkina, E., Gilichinsky, D., Wagener, S., Tiedje, J. & McGrath, J. Biogeochemical activity of anaerobic microorganisms from buried permafrost sediments. Geomicrobiol. J. 15, 187–193 (1998).
Article  Google Scholar 
Hultman, J. et al. Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521, 208–212 (2015).
Article  CAS  PubMed  Google Scholar 
Woodcroft, B. J. et al. Genome-centric view of carbon processing in thawing permafrost. Nature 560, 49–54 (2018).
Article  CAS  PubMed  Google Scholar 
Guglielmin, M., Dalle Fratte, M. & Cannone, N. Permafrost warming and vegetation changes in continental Antarctica. Environ. Res. Lett. 9, 045001 (2014).
Article  Google Scholar 
Goordial, J. et al. Comparative activity and functional ecology of permafrost soils and lithic niches in a hyper‐arid polar desert. Environ. Microbiol. 19, 443–458 (2017).
Article  CAS  PubMed  Google Scholar 
Cook, B. I., Smerdon, J. E., Seager, R. & Coats, S. Global warming and 21st century drying. Clim. Dyn. 43, 2607–2627 (2014).
Article  Google Scholar 
Šťovíček, A., Kim, M., Or, D. & Gillor, O. Microbial community response to hydration-desiccation cycles in desert soil. Sci. Rep. 7, 45735 (2017).
Article  PubMed  PubMed Central  Google Scholar 
Srinivasiah, S. et al. Direct assessment of viral diversity in soils by random PCR amplification of polymorphic DNA. Appl. Environ. Microbiol. 79, 5450–5457 (2013).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Zablocki, O. et al. High-level diversity of tailed phages, eukaryote-associated viruses, and virophage-like elements in the metaviromes of antarctic soils. Appl. Environ. Microbiol. 80, 6888–6897 (2014).
Article  PubMed  PubMed Central  Google Scholar 
Roy Chowdhury, T. et al. Metaphenomic responses of a native prairie soil microbiome to moisture perturbations. mSystems 4, e00061-19 (2019).
Article  PubMed  PubMed Central  Google Scholar 
Michen, B. & Graule, T. Isoelectric points of viruses. J. Appl. Microbiol. 109, 388–397 (2010).
Article  CAS  PubMed  Google Scholar 
Nelson, A. R. et al. Playing with FiRE: a genome resolved view of the soil microbiome responses to high severity forest wildfire. Preprint at bioRxiv https://doi.org/10.1101/2021.08.17.456416 (2021).
Article  PubMed  PubMed Central  Google Scholar 
Braga, L. P. et al. Novel virocell metabolic potential revealed in agricultural soils by virus‐enriched soil metagenome analysis. Environ. Microbiol. Rep. 13, 348–354 (2021).
Article  CAS  PubMed  Google Scholar 
Hwang, Y., Rahlff, J., Schulze-Makuch, D., Schloter, M. & Probst, A. J. Diverse viruses carrying genes for microbial extremotolerance in the Atacama Desert hyperarid soil. mSystems 6, e00385-21 (2021).
Article  PubMed  PubMed Central  Google Scholar 
Ter Horst, A. M. et al. Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations. Microbiome 9, 233 (2021).
Article  PubMed  PubMed Central  Google Scholar 
Van Goethem, M. W., Swenson, T. L., Trubl, G., Roux, S. & Northen, T. R. Characteristics of wetting-induced bacteriophage blooms in biological soil crust. mBio 10, e02287-19 (2019).
Article  PubMed  PubMed Central  Google Scholar 
Kieft, K. et al. Ecology of inorganic sulfur auxiliary metabolism in widespread bacteriophages. Nat. Commun. 12, 1–16 (2021).
Article  Google Scholar 
Nayfach, S. et al. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat. Biotechnol. 39, 578–585 (2021).
Article  CAS  PubMed  Google Scholar 
Lefkowitz, E. J. et al. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res. 46, D708–D717 (2018).
Article  CAS  PubMed  Google Scholar 
Hough, M. et al. Biotic and environmental drivers of plant microbiomes across a permafrost thaw gradient. Front. Microbiol. https://doi.org/10.3389/fmicb.2020.00796 (2020).
Article  PubMed  PubMed Central  Google Scholar 
Naylor, D. et al. Soil microbiomes under climate change and implications for carbon cycling. Annu. Rev. Environ. Resour. 45, 29–59 (2020).
Article  Google Scholar 
Williamson, K. E. et al. Estimates of viral abundance in soils are strongly influenced by extraction and enumeration methods. Biol. Fertil. Soils 49, 857–869 (2013).
Article  Google Scholar 
Graham, E. B. et al. Untapped viral diversity in global soil metagenomes. Preprint at bioRxiv https://doi.org/10.1101/583997 (2019).
Article  Google Scholar 
Shakya, M., Lo, C.-C. & Chain, P. S. Advances and challenges in metatranscriptomic analysis. Front. Genet. 10, 904 (2019).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Steffan, J. J., Derby, J. A. & Brevik, E. C. Soil pathogens that may potentially cause pandemics, including severe acute respiratory syndrome (SARS) coronaviruses. Curr. Opin. Environ. Sci. Health 17, 35–40 (2020).
Article  PubMed  PubMed Central  Google Scholar 
Fortier, L.-C. & Sekulovic, O. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4, 354–365 (2013).
Article  PubMed  PubMed Central  Google Scholar 
Breitbart, M., Miyake, J. H. & Rohwer, F. Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol. Lett. 236, 249–256 (2004).
Article  CAS  PubMed  Google Scholar 
Hassard, F. et al. Abundance and distribution of enteric bacteria and viruses in coastal and estuarine sediments — a review. Front. Microbiol. 7, 1692 (2016).
Article  PubMed  PubMed Central  Google Scholar 
Shade, A. et al. Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3, 417 (2012).
Article  PubMed  PubMed Central  Google Scholar 
Sano, E., Carlson, S., Wegley, L. & Rohwer, F. Movement of viruses between biomes. Appl. Environ. Microbiol. 70, 5842–5846 (2004).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Casteel, M. J., Sobsey, M. D. & Mueller, J. P. Fecal contamination of agricultural soils before and after hurricane-associated flooding in North Carolina. J. Environ. Sci. Health A 41, 173–184 (2006).
Article  CAS  Google Scholar 
Wu, R., Trubl, G., Taş, N. & Jansson, J. K. Permafrost as a potential pathogen reservoir. One Earth 5, 351–360 (2022).
Article  Google Scholar 
Trebicki, P. Climate change and plant virus epidemiology. Virus Res. 286, 198059 (2020).
Article  CAS  PubMed  Google Scholar 
Whitfield, A. E., Falk, B. W. & Rotenberg, D. Insect vector-mediated transmission of plant viruses. Virology 479, 278–289 (2015).
Article  PubMed  Google Scholar 
Velásquez, A. C., Castroverde, C. D. M. & He, S. Y. Plant–pathogen warfare under changing climate conditions. Curr. Biol. 28, R619–R634 (2018).
Article  PubMed  PubMed Central  Google Scholar 
Prasch, C. M. & Sonnewald, U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol. 162, 1849–1866 (2013).
Article  CAS  PubMed  PubMed Central  Google Scholar 
Sutela, S., Poimala, A. & Vainio, E. J. Viruses of fungi and oomycetes in the soil environment. FEMS Microbiol. Ecol. 95, fiz119 (2019).
Article  CAS  PubMed  Google Scholar 
Wang, L. et al. Evidence for a novel negative-stranded RNA mycovirus isolated from the plant pathogenic fungus Fusarium graminearum. Virology 518, 232–240 (2018).
Article  CAS  PubMed  Google Scholar 
Abdoulaye, A. H., Foda, M. F. & Kotta-Loizou, I. Viruses infecting the plant pathogenic fungus Rhizoctonia solani. Viruses 11, 1113 (2019).
Article  CAS  PubMed Central  Google Scholar 
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Research in the laboratory of J.K.J. was supported by the US Department of Energy’s Office of Biological and Environmental Research and is a contribution of the Scientific Focus Area ‘Phenotypic response of the soil microbiome to environmental perturbations’ (FWP 70880). Pacific Northwest National Laboratory is operated for the US Department of Energy by Battelle Memorial Institute under contract DE-AC05-76RLO1830.
Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, USA
Janet K. Jansson & Ruonan Wu
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The authors contributed equally to all aspects of the article.
Correspondence to Janet K. Jansson.
The authors declare no competing interests.
Nature Reviews Microbiology thanks Li-Li Han; Mark Radosevich, who co-reviewed with Xiaolong Liang; and K. Eric Wommack, who co-reviewed with Hannah Locke, for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Global RNA viral data: https://zenodo.org/record/6553771#.YyDwfezML0p
IMG/VR metadata: https://genome.jgi.doe.gov/portal/pages/dynamicOrganismDownload.jsf?organism=IMG_VR
(JGI genome potal log-in is needed) RiboV1.4_Info.tsv: https://portal.nersc.gov/dna/microbial/prokpubs/Riboviria/RiboV1.4/RiboV1.4_Info.tsv
RNA Viruses in Metatranscriptomes database: https://riboviria.org
Virus-Host DB: https://www.genome.jp/virushostdb
Genes carried on soil viruses that are not directly required for viral replication and/or reproduction.
Viruses that have a bacterial host.
An adaptive immunity against foreign elements in many bacteria and most archaea. DNA from the invasive elements (for example viruses) is first taken up and integrated into CRISPR loci as spacers with repeat sequences flanked on both sides. The CRISPR locus is transcribed and modified into mature CRISPR RNA. CRISPR RNA guides the Cas nuclease complex to cleave the sequences after targeted recognition of the invading mobile genetic elements.
Very large double-stranded DNA viruses with genomes as large as or larger than those of some bacteria.
A hypothesis that the temperate phage lifestyle is favoured when host densities are high. Thus, viruses have an opportunity to exploit their hosts via lysogeny instead of lysing them.
Community DNA sequence data that are derived by DNA sequencing.
Community RNA sequence data that are derived by RNA sequencing.
A hypothesis that the dominant bacterial hosts in a system are selectively lysed by phages.
A method used to incorporate stable isotopes into biomolecules and thus to distinguish active cell populations from inactive cell populations (for example, when 18O-labelled H2O is used) or to determine cells that perform a specific metabolic step (for example, when 13C-labelled substrates are used).
Viruses (bacteriophages) that are incorporated into the genome of the bacterial host and display a lysogenic lifestyle.
A term used to describe the largely unknown identities and functions of soil viruses.
Virus-mediated lysis of microbial cells that results in a bypass of the flow of nutrients from microbial cells to higher trophic levels in the soil microbial food web.
Viruses that are extracted from the environment before sequencing.
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Jansson, J.K., Wu, R. Soil viral diversity, ecology and climate change. Nat Rev Microbiol (2022). https://doi.org/10.1038/s41579-022-00811-z
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