Skip to main content
Log in

Applications and limitations of tea extract as a virucidal agent to assess the role of phage predation in soils

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

In marine ecosystems, phage predation (phage-mediated cell lysis) is an important driver of bacterial mortality through host cell death and nutrient cycling through the release of cell contents. Both of these impacts increase marine microbial diversity by increasing interspecific competition. By contrast, very little is known about the role of phage predation in terrestrial ecosystems. A recent field study in Barrow, AK found phage predation to be a key factor controlling terrestrial bacterial population dynamics in Arctic soils. When phage abundance was artificially reduced using a tea extract, antiphage treatment, bacterial abundance, and respiration increased accordingly, suggesting top-down control by phages. The goal of this study was to examine the impact of phage predation in temperate soil ecosystems. Laboratory-scale experiments confirmed the potent antiphage properties of tea extracts. However, field experiments conducted at two discrete sites (upland and wetland) yielded little evidence that top-down control by phage predation was significant in temperate soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Allen B, Willner D, Oechel WC, Lipson D (2010) Top-down control of microbial activity and biomass in an Arctic soil ecosystem. Environ Microbiol 12:642–648. doi:10.1111/j.1462-2920.2009.02104.x

    Article  CAS  PubMed  Google Scholar 

  • Ashelford KE, Day MJ, Bailey MJ, Lilley AK, Fry JC (1999a) In situ population dynamics of bacterial viruses in a terrestrial environment. Appl Environ Microbiol 65:169–174

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ashelford KE, Fry JC, Bailey MJ, Jeffries AR, Day MJ (1999b) Characterization of six bacteriophages of Serratia liquefaciens CP6 isolated from the sugar beet phytosphere. Appl Environ Microbiol 65:1959–1965

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ashelford KE, Norris SJ, Fry JC, Bailey MJ, Day MJ (2000) Seasonal population dynamics and interactions of competing bacteriophages and their host in the rhizosphere. Appl Environ Microbiol 66:4193–4199

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bandara N, Jo J, Ryu S, Kim KP (2012) Bacteriophages BCP1-1 and BCP8-2 require divalent cations for efficient control of Bacillus cereus in fermented foods. Food Microbiol 31:9–16. doi:10.1016/j.fm.2012.02.003

    Article  CAS  PubMed  Google Scholar 

  • Bettarel Y, Amblard C, Sime-Ngando T, Carrias JF, Sargos D, Garabetian F, Lavandier P (2003) Viral lysis, flagellate grazing potential, and bacterial production in Lake Pavin. Microb Ecol 45:119–127. doi:10.1007/s00248-002-1016-1

    Article  CAS  PubMed  Google Scholar 

  • Bonilla-Findji O, Herndl GJ, Gattuso JP, Weinbauer MG (2009) Viral and flagellate control of prokaryotic production and community structure in offshore Mediterranean waters. Appl Environ Microbiol 75:4801–4812. doi:10.1128/aem.01376-08

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bouvier T, del Giorgio PA (2007) Key role of selective viral-induced mortality in determining marine bacterial community composition. Environ Microbiol 9:287–297. doi:10.1111/j.1462-2920.2006.01137.x

    Article  CAS  PubMed  Google Scholar 

  • Bratbak G, Heldal M, Thingstad TF, Riemann B, Haslund OH (1992) Incorporation of viruses into the budget of microbial C-transfer. A first approach. Mar Ecol Prog Ser 83:273–280

    Article  Google Scholar 

  • Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–149. doi:10.1007/s00374-011-0653-2

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clarholm M (1981) Protozoan grazing of bacteria in soil—impact and importance. Microb Ecol 7:343–350

    Article  CAS  PubMed  Google Scholar 

  • Cochlan WP, Wikner J, Steward GF, Smith DC, Azam F (1993) Spatial distribution of viruses, bacteria, and chlorophyll a in neritic, oceanic and estuarine environments. Mar Ecol Progr Ser 92:77–87

    Article  Google Scholar 

  • De Siqueira RS, Dodd CER, Rees CED (2006) Evaluation of the natural virucidal activity of teas for use in the phage amplification assay. Int J Food Microbiol 111:259–262. doi:10.1016/j.ijfoodmicro.2006.04.047

    Article  PubMed  Google Scholar 

  • Friedman M (2007) Overview of antibacterial, antitoxin, antiviral, and antifungal activities of tea flavonoids and teas. Mol Nutr Food Res 51:116–134. doi:10.1002/mnfr.200600173

    Article  CAS  PubMed  Google Scholar 

  • Hatfull GF, Russell DA, Pope WH, Jacobs-Sera D, Tse E, Fabricant S (2010a) The Mycobacteriophage Database, details for phage larva. In: the Mycobacteriophage Database. http://phagesdb.org/phages/Larva/. Accessed 5 May 2013

  • Hatfull GF, Russell DA, Pope WH, Jacobs-Sera D, Tse E, Fabricant S (2010b) The Mycobacteriophage Database, details for phage doom. In: the Mycobacteriophage Database. http://phagesdb.org/phages/Doom/. Accessed 5 May 2013

  • Hider RC, Liu ZD, Khodr HH (2001) Metal chelation of polyphenols. Methods Enzymol 335:190–203

    CAS  PubMed  Google Scholar 

  • Hill BH, Elonen CM, Jicha TM, Cotter AM, Trebitz AS, Danz NP (2006) Sediment microbial enzyme activity as an indicator of nutrient limitation in Great Lakes coastal wetlands. Freshwater Biol 51:1670–1683. doi:10.1111/j.1365-2427.2006.01606.x

    Article  CAS  Google Scholar 

  • Jensen LS, Sorensen J (1994) Microscale fumigation-extraction and substrate-induced respiration methods for measuring microbial biomass in barley rhizosphere. Plant Soil 162:151–161. doi:10.1007/bf01347701

    Article  CAS  Google Scholar 

  • Judd KE, Crump BC, Kling GW (2006) Variation in dissolved organic matter controls bacterial production and community composition. Ecology 87:2068–2079. doi:10.1890/0012-9658(2006)87[2068:vidomc]2.0.co;2

    Article  PubMed  Google Scholar 

  • Kizildag N, Aka Sagliker H, Darici C (2012) Comparison of the effects of tannin and azadirachtin on carbon mineralization in soils of Quercus coccifera from eastern Mediterranean region. Ekoloji 21:47–53. doi:10.5053/ekoloji.2011.846

    Article  CAS  Google Scholar 

  • Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PG, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek 81:509–520. doi:10.1023/a:1020565523615

    Article  PubMed  Google Scholar 

  • Kramer S, Green DM (2000) Acid and alkaline phosphatase dynamics and their relationship to soil microclimate in a semiarid woodland. Soil Biol Biochem 32:179–188. doi:10.1016/S0038-0717(99)00140-6

    Article  CAS  Google Scholar 

  • Miki T, Nakazawa T, Yokokawa T, Nagata T (2008) Functional consequences of viral impacts on bacterial communities: a food-web model analysis. Freshwater Biol 53:1142–1153. doi:10.1111/j.1365-2427.2007.01934.x

    Article  Google Scholar 

  • Mikola J, Setala H (1998) No evidence of trophic cascades in an experimental microbial-based soil food web. Ecology 79:153–164. doi:10.2307/176871

    Article  Google Scholar 

  • Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762. doi:10.1007/s00374-012-0723-0

    Article  Google Scholar 

  • Pope WH, Ferreira CM, Jacobs-Sera D, Benjamin RC, Davis AJ, DeJong RJ, Elgin SCR, Guilfoile FR, Forsyth MH, Harris AD, Harvey SE, Hughes LE, Hynes PM, Jackson AS, Jalal MD, MacMurray EA, Manley CM, McDonough MJ, Mosier JL, Osterbann LJ, Rabinowitz HS, Rhyan CN, Russell DA, Saha MS, Shaffer CD, Simon SE, Sims EF, Tovar IG, Weisser EG, Wertz JT, Weston-Hafer KA, Williamson KE, Zhang B, Cresawn SG, Jain P, Piuri M, Jacobs WR, Hendrix RW, Hatfull GF (2011) Cluster K mycobacteriophages: insights into the evolutionary origins of mycobacteriophage TM4. PLoS ONE 6:e26750. doi:10.1371/journal.pone.0026750

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Quiberoni A, Reinheimer JA (1998) Physicochemical characterization of phage adsorption to Lactobacillus helveticus ATCC 15807 cells. J Appl Microbiol 85:762–768. doi:10.1111/j.1365-2672.1998.00591.x

    Article  Google Scholar 

  • Rosenberg K, Bertaux J, Krome K, Hartmann A, Scheu S, Bonkowski M (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME J 3:675–684

    Article  CAS  PubMed  Google Scholar 

  • Sandaa RA, Gomez-Consarnau L, Pinhassi J, Riemann L, Malits A, Weinbauer MG, Gasol JM, Thingstad TF (2009) Viral control of bacterial biodiversity—evidence from a nutrient-enriched marine mesocosm experiment. Environ Microbiol 11:2585–2597. doi:10.1111/j.1462-2920.2009.01983.x

    Article  CAS  PubMed  Google Scholar 

  • Scheu S, Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone: manipulation of food resources. Ecology 79:1573–1585

    Article  Google Scholar 

  • Shein EV, Devin BA (2007) Current problems in the study of colloidal transport in soil. Eurasian Soil Sci 40:399–408. doi:10.1134/s1064229307040059

    Article  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. doi:10.1111/j.1461-0248.2008.01245.x

    PubMed  Google Scholar 

  • Srinivasiah S, Bhavsar J, Thapar K, Liles M, Schoenfeld T, Wommack KE (2008) Phages across the biosphere: contrasts of viruses in soil and aquatic environments. Res Microbiol 159:349–357

    Article  CAS  PubMed  Google Scholar 

  • Stewart GSAB, Jassim SAA, Denyer SP, Newby P, Linley K, Dhir VK (1998) The specific and sensitive detection of bacterial pathogens within 4 h using bacteriophage amplification. J Appl Microbiol 84:777–783

    Google Scholar 

  • Thingstad TF (2000) 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

    Article  Google Scholar 

  • Turner BL, Baxter R, Whitton BA (2002) Seasonal phosphatase activity in three characteristic soils of the English uplands polluted by long-term atmospheric nitrogen deposition. Environ Pollut 120:313–317. doi:10.1016/S0269-7491(02)00147-1

    Article  CAS  PubMed  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) Microbial biomass measurements in forest soils-the use of the chloroform fumigation incubation methods in strongly acid soils. Soil Biol Biochem 19:697–702. doi:10.1016/0038-0717(87)90051-4

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Weinbauer MG, Hofle MG (1998) Size-specific mortality of lake bacterioplankton by natural virus communities. Aquat Microb Ecol 15:103–113

    Article  Google Scholar 

  • Wen K, Ortmann AC, Suttle CA (2004) Accurate estimation of viral abundance by epifluorescence microscopy. Appl Env Microbiol 70:3862–3867

    Article  CAS  Google Scholar 

  • Williamson KE (2011) Soil phage ecology: abundance, distribution, and interactions with bacterial hosts. In: Witzany G (ed) Biocommunication in soil microorganisms. Springer, Berlin, pp 113–136

    Chapter  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Williamson KE, Kan J, Polson SW, Williamson SJ (2011) Optimizing the indirect extraction of prokaryotic DNA from soils. Soil Biol Biochem 43:736–748. doi:10.1016/j.soilbio.2010.04.017

    Article  CAS  Google Scholar 

  • Williamson KE, Srinivasiah S, Wommack KE (2012) Viruses. In: Huang PM, Li Y, Sumner ME (eds) Handbook of soil science. Taylor and Francis, New York, pp 24-1–24-8

    Google Scholar 

  • Williamson KE, Corzo KA, Drissi CL, Buckingham JM, Thompson CP, Helton RR (2013) Estimates of viral abundance in soils are strongly influenced by extraction and enumeration methods. Biol Fertil Soils. doi:10.1007/s00374-013-0780-z

    Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by William & Mary Honors Funding to KRH provided by individual donors Dr. John Sherwood, Ms. Margery Daughtry, Mr. Ted Dintersmith, and Ms. Janet Bouland and by a grant to KEW from the Jeffress Memorial Trust (J-988). We would like to thank Carl Zimmerman at Chesapeake Biological Laboratory for performing the DOC analyses and M.A. Saxton for helping to improve the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kurt E. Williamson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 620 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Helsley, K.R., Brown, T.M., Furlong, K. et al. 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). https://doi.org/10.1007/s00374-013-0855-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-013-0855-x

Keywords

Navigation