Skip to main content

Diversity and Distribution Characteristics of Viruses in Soils of a Marine-Terrestrial Ecotone in East China

Microbial Ecology volume 75, pages 375–386 (2018)Cite this article

Abstract

A substantial gap remains in our understanding of the abundance, diversity, and ecology of viruses in soil although some advances have been achieved in recent years. In this study, four soil samples according to the salinity gradient from shore to inland in East China have been characterized. Results showed that spherical virus particles represented the largest viral component in all of the four samples. The viromes had remarkably different taxonomic compositions, and most of the sequences were derived from single-stranded DNA viruses, especially from families Microviridae and Circoviridae. Compared with viromes from other aquatic and sediment samples, the community compositions of our four soil viromes resembled each other, meanwhile coastal sample virome closely congregated with sediment and hypersaline viromes, and high salinity paddy soil sample virome was similar with surface sediment virome. Phylogenetic analysis of functional genes showed that four viromes have high diversity of the subfamily Gokushovirinae in family Microviridae and most of Circoviridae replicase protein sequences grouped within the CRESS-DNA viruses. This work provided an initial outline of the viral communities in marine-terrestrial ecotone and will improve our understanding of the ecological functions of soil viruses.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Edwards RA, Rohwer F (2005) Viral metagenomics. Nat Rev Microbiol 3:504–510

    CAS  Article  PubMed  Google Scholar 

  2. Chibani-Chennoufi S, Bruttin A, Dillmann ML, Brussow H (2004) Phage-host interaction: an ecological perspective. J Bacteriol 186:3677–3686

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Suttle CA (2005) Viruses in the sea. Nature 437:356–361

    CAS  Article  PubMed  Google Scholar 

  4. Dennehy JJ (2014) What ecologists can tell virologists. Annu Rev Microbiol 68:117–135

    CAS  Article  PubMed  Google Scholar 

  5. Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea—viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49:781–788

    Article  Google Scholar 

  6. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–548

    CAS  Article  PubMed  Google Scholar 

  8. Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, Azam F, Rohwer F (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99:14250–14255

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Adriaenssens EM, Van Zyl L, De Maayer P, Rubagotti E, Rybicki E, Tuffin M, Cowan DA (2015) Metagenomic analysis of the viral community in Namib Desert hypoliths. Environ Microbiol 17:480–495

    CAS  Article  PubMed  Google Scholar 

  10. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181

    CAS  Article  PubMed  Google Scholar 

  11. Weitz JS, Stock CA, Wilhelm SW, Bourouiba L, Coleman ML, Buchan A, Follows MJ, Fuhrman JA, Jover LF, Lennon JT, Middelboe M, Sonderegger DL, Suttle CA, Taylor BP, Thingstad TF, Wilson WH, Wommack KE (2015) A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J 9:1352–1364

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hurwitz BL, Sullivan MB (2013) The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS One 8(2):e57355

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Mizuno CM, Rodriguez-Valera F, Kimes NE, Ghai R (2013) Expanding the marine virosphere using metagenomics. PLoS Genet 9:e1003987

    Article  PubMed  PubMed Central  Google Scholar 

  14. Yoshida M, Takaki Y, Eitoku M, Nunoura T, Takai K (2013) Metagenomic analysis of viral communities in (hado)pelagic sediments. PLoS One 8(2):e57271

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Zablocki O, Adriaenssens EM, Cowan D (2016) Diversity and ecology of viruses in hyperarid desert soils. Appl Environ Microbiol 82:770–777

    CAS  Article  PubMed Central  Google Scholar 

  16. Reavy B, Swanson MM, Cock PJA, Dawson L, Freitag TE, Singh BK, Torrance L, Mushegian AR, Taliansky M (2015) Distinct circular single-stranded DNA viruses exist in different soil types. Appl Environ Microbiol 81:3934–3945

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Hatfull GF, Hendrix RW (2011) Bacteriophages and their genomes. Curr Opin Virol 1:298–303

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Hendrix RW (2002) Bacteriophages: evolution of the majority. Theor Popul Biol 61:471–480

    Article  PubMed  Google Scholar 

  19. Miller RV (2001) Environmental bacteriophage-host interactions: factors contribution to natural transduction. Anton Leeuw Int J G 79:141–147

    CAS  Article  Google Scholar 

  20. Williamson KE, Wommack KE, Radosevich M (2003) Sampling natural viral communities from soil for culture-independent analyses. Appl Environ Microbiol 69:6628–6633

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Patel A, Noble RT, Steele JA, Schwalbach MS, Hewson I, Fuhrman JA (2007) Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I. Nat Protoc 2:269–276

    CAS  Article  PubMed  Google Scholar 

  22. Wommack KE, Hill RT, Kessel M, Russekcohen E, Colwell RR (1992) Distribution of viruses in the Chesapeake Bay. Appl Environ Microbiol 58:2965–2970

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Zablocki O, van Zyl L, Adriaenssens EM, Rubagotti E, Tuffin M, Cary SC, Cowan D (2014) 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

    Article  PubMed  PubMed Central  Google Scholar 

  24. Dean FB, Nelson JR, Giesler TL, Lasken RS (2001) Rapid amplification of plasmid and phage DNA using phi29 DNA polymerase and multiply-primed rolling circle amplification. Genome Res 11:1095–1099

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Wilke A, Bischof J, Gerlach W, Glass E, Harrison T, Keegan KP, Paczian T, Trimble WL, Bagchi S, Gram A, Chaterji S, Meyer F (2016) The MG-RAST metagenomics database and portal in 2015. Nucleic Acids Res 44:D590–D594

    CAS  Article  PubMed  Google Scholar 

  26. Li RQ, Zhu HM, Ruan J, Qian WB, Fang XD, Shi ZB, Li YR, Li ST, Shan G, Kristiansen K, Li SG, Yang HM, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Roux S, Faubladier M, Mahul A, Paulhe N, Bernard A, Debroas D, Enault F (2011) Metavir: a web server dedicated to virome analysis. Bioinformatics 27:3074–3075

    CAS  Article  PubMed  Google Scholar 

  28. Wilke A, Bischof J, Harrison T, Brettin T, D'Souza M, Gerlach W, Matthews H, Paczian T, Wilkening J, Glass EM, Desai N, Meyer F (2015) A RESTful API for accessing microbial community data for MG-RAST. PLoS Comput Biol 11(1):e1004008

    Article  PubMed  PubMed Central  Google Scholar 

  29. Ondov BD, Bergman NH, Phillippy AM (2011) Interactive metagenomic visualization in a Web browser. BMC Bioinf 12:385

    Article  Google Scholar 

  30. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Quaiser A, Dufresne A, Ballaud F, Roux S, Zivanovic Y, Colombet J, Sime-Ngando T, Francez AJ (2015) Diversity and comparative genomics of Microviridae in Sphagnum-dominated peatlands. Front Microbiol 6:375

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rosario K, Dayaram A, Marinov M, Ware J, Kraberger S, Stainton D, Breitbart M, Varsani A (2012) Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). J Gen Virol 93:2668–2681

    CAS  Article  PubMed  Google Scholar 

  33. Williamson KE, Radosevich M, Wommack KE (2005) Abundance and diversity of viruses in six Delaware soils. Appl Environ Microbiol 71:3119–3125

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Swanson MM, Fraser G, Daniell TJ, Torrance L, Gregory PJ, Taliansky M (2009) Viruses in soils: morphological diversity and abundance in the rhizosphere. Ann Appl Biol 155:51–60

    Article  Google Scholar 

  35. Wichman HA, Brown CJ (2010) Experimental evolution of viruses: Microviridae as a model system. Philos Trans R Soc B 365:2495–2501

    CAS  Article  Google Scholar 

  36. Ackermann HW (2007) 5500 phages examined in the electron microscope. Arch Virol 152:227–243

    CAS  Article  PubMed  Google Scholar 

  37. Ackermann HW (1996) Frequency of morphological phage descriptions in 1995. Arch Virol 141:209–218

    CAS  Article  PubMed  Google Scholar 

  38. Ackermann HW (2001) Frequency of morphological phage descriptions in the year 2000. Arch Virol 146:843–857

    CAS  Article  PubMed  Google Scholar 

  39. Tucker KP, Parsons R, Symonds EM, Breitbart M (2011) Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean. ISME J 5:822–830

    CAS  Article  PubMed  Google Scholar 

  40. Roux S, Enault F, Robin A, Ravet V, Personnic S, Theil S, Colombet J, Sime-Ngando T, Debroas D (2012) Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS One 7(3):e33641

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Labonte JM, Suttle CA (2013) Metagenomic and whole-genome analysis reveals new lineages of gokushoviruses and biogeographic separation in the sea. Front Microbiol 5:52

    Google Scholar 

  42. Roux S, Krupovic M, Poulet A, Debroas D, Enault F (2012) Evolution and diversity of the Microviridae viral family through a collection of 81 new complete genomes assembled from virome reads. PLoS One 7(7):e40418

    Article  PubMed  PubMed Central  Google Scholar 

  43. Zhong X, Guidoni B, Jacas L, Jacquet S (2015) Structure and diversity of ssDNA Microviridae viruses in two peri-alpine lakes (Annecy and Bourget, France). Res Microbiol 166:644–654

    CAS  Article  PubMed  Google Scholar 

  44. Varsani A, Navas-Castillo J, Moriones E, Hernandez-Zepeda C, Idris A, Brown JK, Zerbini FM, Martin DP (2014) Establishment of three new genera in the family Geminiviridae: Becurtovirus, Eragrovirus and Turncurtovirus. Arch Virol 159:2193–2203

    CAS  Article  PubMed  Google Scholar 

  45. Kim KH, Chang HW, Nam YD, Roh SW, Kim MS, Sung Y, Jeon CO, Oh HM, Bae JW (2008) Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl Environ Microbiol 74:5975–5985

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Cassman N, Prieto-Davo A, Walsh K, Silva GGZ, Angly F, Akhter S, Barott K, Busch J, McDole T, Haggerty JM, Willner D, Alarcon G, Ulloa O, DeLong EF, Dutilh BE, Rohwer F, Dinsdale EA (2012) Oxygen minimum zones harbour novel viral communities with low diversity. Environ Microbiol 14:3043–3065

    CAS  Article  PubMed  Google Scholar 

  47. Guercio A, Savini F, Casa G, Di Marco P, Purpari G, Cannella V, Puleio R, Lavazza A, Buttaci C, Piquemal D, Trentin B, Morent M, Scagliarini A (2014) Massive proliferative cutaneous lesions associated with Poxviridae and Papillomaviridaeviral species in ruminants. Int J Infect Dis 21:183–184

    Article  Google Scholar 

  48. Fierer N, Breitbart M, Nulton J, Salamon P, Lozupone C, Jones R, Robeson M, Edwards RA, Felts B, Rayhawk S, Knight R, Rohwer F, Jackson RB (2007) Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, archaea, fungi, and viruses in soil. Appl Environ Microbiol 73:7059–7066

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, Furlan M, Desnues C, Haynes M, Li LL, McDaniel L, Moran MA, Nelson KE, Nilsson C, Olson R, Paul J, Brito BR, Ruan YJ, Swan BK, Stevens R, Valentine DL, Thurber RV, Wegley L, White BA, Rohwer F (2008) Functional metagenomic profiling of nine biomes. Nature 452:629–632

    CAS  Article  PubMed  Google Scholar 

  50. Chow CET, Suttle CA (2015) Biogeography of viruses in the sea. Annu Rev Virol 2:41–66

    CAS  Article  PubMed  Google Scholar 

  51. Angly FE, Felts B, Breibart M, Salamon P, Edwards RA, Carlson C, Chan AM, Haynes M, Kelley S, Liu H, Mahaffy JM, Mueller JE, Nulton J, Rohwer F (2006) The marine viromes of four oceanic regions. PLoS Biol 4:2121–2131

    CAS  Article  Google Scholar 

  52. Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F (2009) Laboratory procedures to generate viral metagenomes. Nat Protoc 4:470–483

    CAS  Article  PubMed  Google Scholar 

  53. Haible D, Kober S, Jeske H (2006) Rolling circle amplification revolutionizes diagnosis and genomics of geminiviruses. J Virol Methods 135:9–16

    CAS  Article  PubMed  Google Scholar 

  54. Kim KH, Bae JW (2011) Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol 77:7663–7668

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Lizardi PM, Huang XH, Zhu ZR, Bray-Ward P, Thomas DC, Ward DC (1998) Mutation detection and single-molecule counting using isothermal rolling-circle amplification. Nat Genet 19:225–232

    CAS  Article  PubMed  Google Scholar 

  56. Lopez-Bueno A, Tamames J, Velazquez D, Moya A, Quesada A, Alcami A (2009) High diversity of the viral community from an Antarctic Lake. Science 326:858–861

    CAS  Article  PubMed  Google Scholar 

  57. Rosario K, Nilsson C, Lim YW, Ruan YJ, Breitbart M (2009) Metagenomic analysis of viruses in reclaimed water. Environ Microbiol 11:2806–2820

    CAS  Article  PubMed  Google Scholar 

  58. Reyes A, Haynes M, Hanson N, Angly FE, Heath AC, Rohwer F, Gordon JI (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466:334–381

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. Rodriguez-Brito B, Li LL, Wegley L, Furlan M, Angly F, Breitbart M, Buchanan J, Desnues C, Dinsdale E, Edwards R, Felts B, Haynes M, Liu H, Lipson D, Mahaffy J, Martin-Cuadrado AB, Mira A, Nulton J, Pasic L, Rayhawk S, Rodriguez-Mueller J, Rodriguez-Valera F, Salamon P, Srinagesh S, Thingstad TF, Tran T, Thurber RV, Willner D, Youle M, Rohwer F (2010) Viral and microbial community dynamics in four aquatic environments. ISME J 4:739–751

    Article  PubMed  Google Scholar 

  60. Fancello L, Trape S, Robert C, Boyer M, Popgeorgiev N, Raoult D, Desnues C (2013) Viruses in the desert: a metagenomic survey of viral communities in four perennial ponds of the Mauritanian Sahara. ISME J 7:359–369

    CAS  Article  PubMed  Google Scholar 

  61. Han LL, Yu DT, Zhang LM, Wang JT, He JZ (2017) Unique community structure of viruses in a glacier soil of the Tianshan Mountains, China. J Soil Sediment 17:852–860

    CAS  Article  Google Scholar 

  62. Han LL, Yu DT, Zhang LM, Shen JP, He JZ (2017) Genetic and functional diversity of ubiquitous DNA viruses in selected Chinese agricultural soils. Sci Report 7:45142

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation of China (Grant Nos. 41771289 and 41571248).

Author information

Affiliations

  1. State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Dan-Ting Yu, Li-Li Han, Li-Mei Zhang & Ji-Zheng He

  2. University of the Chinese Academy of Sciences, Beijing, 100049, China

    Dan-Ting Yu, Li-Li Han, Li-Mei Zhang & Ji-Zheng He

  3. Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, Victoria, 3010, Australia

    Ji-Zheng He

Authors
  1. Dan-Ting Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Li-Li Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li-Mei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ji-Zheng He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Li-Li Han or Ji-Zheng He.

Electronic Supplementary Material

ESM 1

(XLSX 36 kb)

ESM 2

(PPTX 1172 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yu, DT., Han, LL., Zhang, LM. et al. Diversity and Distribution Characteristics of Viruses in Soils of a Marine-Terrestrial Ecotone in East China. Microb Ecol 75, 375–386 (2018). https://doi.org/10.1007/s00248-017-1049-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1049-0

Keywords

  • Viruses
  • Virome
  • Marine-terrestrial ecotone
  • Capsid protein
  • Replicase protein