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  • Review article
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Soil viral diversity, ecology and climate change

Abstract

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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Fig. 1: Taxonomic composition of soil DNA and RNA viruses and their known hosts.
Fig. 2: Different aspects of soil viral ecology and lifestyles.
Fig. 3: Impacts of permafrost thaw on soil viruses.
Fig. 4: Impacts of changes in soil moisture on soil viruses.

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References

  1. 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 

  2. Suttle, C. A. Marine viruses — major players in the global ecosystem. Nat. Rev. Microbiol. 5, 801–812 (2007).

    Article  CAS  PubMed  Google Scholar 

  3. 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 

  4. 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 

  5. 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 

  6. 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 

  7. 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 

  8. 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 

  9. 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 

  10. 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 

  11. 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 

  12. 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 

  13. Jansson, J. K. & Hofmockel, K. S. Soil microbiomes and climate change. Nat. Rev. Microbiol. 18, 35–46 (2020).

    Article  CAS  PubMed  Google Scholar 

  14. 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 

  15. 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 

  16. 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 

  17. 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 

  18. 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 

  19. 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 

  20. 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 

  21. 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 

  22. 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 

  23. 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 

  24. Paez-Espino, D. et al. Uncovering Earth’s virome. Nature 536, 425–430 (2016).

    Article  CAS  PubMed  Google Scholar 

  25. 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 

  26. 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 

  27. 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 

  28. 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 

  29. 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 

  30. 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 

  31. 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 

  32. 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 

  33. 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 

  34. Swanson, M. et al. Viruses in soils: morphological diversity and abundance in the rhizosphere. Ann. Appl. Biol. 155, 51–60 (2009).

    Article  Google Scholar 

  35. Wu, R. et al. Moisture modulates soil reservoirs of active DNA and RNA viruses. Commun. Biol. 4, 1–11 (2021).

    Article  Google Scholar 

  36. Trubl, G. et al. Soil viruses are underexplored players in ecosystem carbon processing. mSystems 3, e00076-18 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  37. 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 

  38. Fischer, M. G. Giant viruses come of age. Curr. Opin. Microbiol. 31, 50–57 (2016).

    Article  PubMed  Google Scholar 

  39. Raoult, D. et al. The 1.2-megabase genome sequence of Mimivirus. Science 306, 1344–1350 (2004).

    Article  CAS  PubMed  Google Scholar 

  40. Pagnier, I. et al. A decade of improvements in Mimiviridae and Marseilleviridae isolation from amoeba. Intervirology 56, 354–363 (2013).

    Article  PubMed  Google Scholar 

  41. 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 

  42. 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 

  43. 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 

  44. 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 

  45. Schulz, F. et al. Hidden diversity of soil giant viruses. Nat. Commun. 9, 4881 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  46. 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 

  47. Hulo, C. et al. ViralZone: a knowledge resource to understand virus diversity. Nucleic Acids Res. 39, D576–D582 (2011).

    Article  CAS  PubMed  Google Scholar 

  48. 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 

  49. 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 

  50. 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 

  51. 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 

  52. Roux, S. et al. Minimum information about an uncultivated virus genome (MIUViG). Nat. Biotechnol. 37, 29–37 (2019).

    Article  CAS  PubMed  Google Scholar 

  53. 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 

  54. 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 

  55. 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 

  56. 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 

  57. 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 

  58. 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 

  59. Peck, K. M. & Lauring, A. S. Complexities of viral mutation rates. J. Virol. 92, e01031-17 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Malathi, V. & Renuka Devi, P. ssDNA viruses: key players in global virome. Virusdisease 30, 3–12 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. 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 

  62. 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 

  63. 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 

  64. 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 

  65. 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 

  66. 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 

  67. 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 

  68. 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  PubMed Central  Google Scholar 

  69. 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 

  70. 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 

  71. 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 

  72. 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 

  73. 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 

  74. 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 

  75. Knowles, B. et al. Lytic to temperate switching of viral communities. Nature 531, 466–470 (2016).

    Article  CAS  PubMed  Google Scholar 

  76. 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 

  77. 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 

  78. 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 

  79. 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 

  80. 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 

  81. 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 

  82. 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 

  83. 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 

  84. 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 

  85. 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 

  86. 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 

  87. 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 

  88. 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 

  89. Paterson, S. et al. Antagonistic coevolution accelerates molecular evolution. Nature 464, 275–278 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317–327 (2010).

    Article  CAS  PubMed  Google Scholar 

  91. 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 

  92. 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 

  93. Poisot, T., Lounnas, M. & Hochberg, M. E. The structure of natural microbial enemy-victim networks. Ecol. Process. 2, 13 (2013).

    Article  Google Scholar 

  94. Trubl, G. et al. Active virus-host interactions at sub-freezing temperatures in Arctic peat soil. Microbiome 9, 1–15 (2021).

    Article  Google Scholar 

  95. 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 

  96. 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 

  97. 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 

  98. 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  PubMed Central  Google Scholar 

  99. 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 

  100. 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 

  101. 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 

  102. Jin, M. et al. Diversities and potential biogeochemical impacts of mangrove soil viruses. Microbiome 7, 58 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  103. 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 

  104. 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 

  105. 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 

  106. 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 

  107. 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 

  108. 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 

  109. 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 

  110. Yeager, J. & O’Brien, R. Enterovirus inactivation in soil. Appl. Environ. Microbiol. 38, 694–701 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Reanney, D. & Marsh, S. The ecology of viruses attacking Bacillus stearothermophilus in soil. Soil Biol. Biochem. 5, 399–408 (1973).

    Article  Google Scholar 

  112. 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 

  113. 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 

  114. 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 

  115. Jansson, J. K. & Taş, N. The microbial ecology of permafrost. Nat. Rev. Microbiol. 12, 414–425 (2014).

    Article  CAS  PubMed  Google Scholar 

  116. 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 

  117. 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 

  118. 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 

  119. Mondav, R. et al. Discovery of a novel methanogen prevalent in thawing permafrost. Nat. Commun. 5, 3212 (2014).

    Article  PubMed  Google Scholar 

  120. 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 

  121. 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 

  122. Woodcroft, B. J. et al. Genome-centric view of carbon processing in thawing permafrost. Nature 560, 49–54 (2018).

    Article  CAS  PubMed  Google Scholar 

  123. Guglielmin, M., Dalle Fratte, M. & Cannone, N. Permafrost warming and vegetation changes in continental Antarctica. Environ. Res. Lett. 9, 045001 (2014).

    Article  Google Scholar 

  124. 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 

  125. 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 

  126. 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 

  127. 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 

  128. 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 

  129. 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 

  130. Michen, B. & Graule, T. Isoelectric points of viruses. J. Appl. Microbiol. 109, 388–397 (2010).

    Article  CAS  PubMed  Google Scholar 

  131. 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 

  132. 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 

  133. 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 

  134. 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 

  135. 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 

  136. Kieft, K. et al. Ecology of inorganic sulfur auxiliary metabolism in widespread bacteriophages. Nat. Commun. 12, 1–16 (2021).

    Article  Google Scholar 

  137. 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 

  138. 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 

  139. 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 

  140. 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 

  141. 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 

  142. 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 

  143. 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 

  144. 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 

  145. 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 

  146. 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 

  147. 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 

  148. Shade, A. et al. Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3, 417 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  149. 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 

  150. 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 

  151. Wu, R., Trubl, G., Taş, N. & Jansson, J. K. Permafrost as a potential pathogen reservoir. One Earth 5, 351–360 (2022).

    Article  Google Scholar 

  152. Trebicki, P. Climate change and plant virus epidemiology. Virus Res. 286, 198059 (2020).

    Article  CAS  PubMed  Google Scholar 

  153. Whitfield, A. E., Falk, B. W. & Rotenberg, D. Insect vector-mediated transmission of plant viruses. Virology 479, 278–289 (2015).

    Article  PubMed  Google Scholar 

  154. 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 

  155. 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 

  156. 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 

  157. 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 

  158. Abdoulaye, A. H., Foda, M. F. & Kotta-Loizou, I. Viruses infecting the plant pathogenic fungus Rhizoctonia solani. Viruses 11, 1113 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

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.

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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.

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Related links

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

Supplementary information

Glossary

Auxiliary metabolic genes (AMGs)

Genes carried on soil viruses that are not directly required for viral replication and/or reproduction.

Bacteriophages

Viruses that have a bacterial host.

CRISPR–Cas

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.

Giant viruses

Very large double-stranded DNA viruses with genomes as large as or larger than those of some bacteria.

Kill-the-winner hypothesis

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.

Metagenome

Community DNA sequence data that are derived by DNA sequencing.

Metatranscriptome

Community RNA sequence data that are derived by RNA sequencing.

Piggyback-the-winner hypothesis

A hypothesis that the dominant bacterial hosts in a system are selectively lysed by phages.

Stable-isotope probing

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).

Temperate phages

Viruses (bacteriophages) that are incorporated into the genome of the bacterial host and display a lysogenic lifestyle.

Viral ‘dark matter’

A term used to describe the largely unknown identities and functions of soil viruses.

Viral shunt

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.

Viromes

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 21, 296–311 (2023). https://doi.org/10.1038/s41579-022-00811-z

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