Phage Biopesticides and Soil Bacteria: Multilayered and Complex Interactions

  • Antonet M. Svircev
  • Susan M. Lehman
  • Peter Sholberg
  • Dwayne Roach
  • Alan J. Castle
Chapter
First Online:
Part of the Soil Biology book series (SOILBIOL, volume 23)

Abstract

Soil ecosystems are impacted by the application of biological control agents to aerial portions of plants. The use of bacteriophages, “phages,” as agriculture biopesticides has been adopted and utilized in a number of host–pathogen systems. Phages may be applied as aerial sprays, preplant treatments and soil drenches in concentrations up to 108–10PFU/ml. The short- and long-term ecology of local soil microbial communities may be impacted by the use of phages since the soil ecosystem provides a suitable template for phage–bacterial interactions. The soil rhizosphere is modulated by exudates from plant roots that allow the development of bacterial populations and interaction with phages. Phages likely regulate host populations by lysis but may compensate by having longer lysogenic stages that prevent further infection and lysis. Phages appear to be large reservoirs of genes that encode proteins that may be novel to any bacterial strain. Studies with both virulent and lysogenic phage gene sequences show that phage–bacterial interactions that occur in soil permit genetic exchange from one host to another. The exchanges may involve the exchange of genetic material via lysogeny, lytic action, abortive infections, transduction, and pseudolysogeny.

The chapter presents three specific case studies that highlight interaction between indigenous soil bacteria, plant pathogens or symbionts (Erwinia amylovora, Pectobacterium carotovorum, and Rhizobacteria), and bacteriophages applied as biological control agents. In addition, we address the special role of lysogeny in the soil–phage interactions and the current methods employed for the detection of phages in the soil.

Keywords

Phage Type Fire Blight Bacterial Host Orchard Soil Pectobacterium Carotovorum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

References

  1. Abebe HM, Sadowsky MJ, Kinkle BK, Schmidt EL (1992) Lysogeny in Bradyrhizobium japonicum and its effect on soybean nodulation. Appl Environ Microbiol 58:3360–3366PubMedGoogle Scholar
  2. Abedon ST (2008) Phage, ecology, and evolution. In: Abedon ST (ed) Bacteriophage ecology. Advances in molecular and cellular microbiology, vol 15. Cambridge University Press, Cambridge UK, pp 1–28Google Scholar
  3. Adams MH (1959) Bacteriophages. Interscience Publishers, New YorkGoogle Scholar
  4. Ahokas H, Erkkila MJ (1993) Interference of PCR amplification by the polyamines, spermine and spermidine. PCR Methods Appl 3:65–68PubMedGoogle Scholar
  5. Andrews JH, Harris RF (2000) The ecology and biogeography of microorganisms on plant surfaces. Ann Rev Phytopathol 38:145–180Google Scholar
  6. Ashelford KE, Day MJ, Bailey MJ, Lilley AK, Fry JC (1999) In situ population dynamics of bacterial viruses in a terrestrial environment. Appl Environ Microbiol 65:169–174PubMedGoogle Scholar
  7. Ashelford KE, Day MJ, Fry JC (2003) Elavated abundance of bacteriophage infecting bacteria in soil. Appl Environ Microbiol 69:285–289PubMedGoogle Scholar
  8. Assadian NW, Giovanni GD, Enciso J, Iglesias J, Lindemann W (2005) The transport of waterborne solutes and bacteriophage in soil subirrigated with a wastewater blend. Agric Ecosyst Environ 111:279–291Google Scholar
  9. Bachoon DS, Otero E, Hodson RE (2001) Effects of humic substances on fluorometric DNA quantification and DNA hybridization. J Microbiol Methods 47:73–82PubMedGoogle Scholar
  10. Balogh B, Canteros BI, Stall RE, Jones JB (2008) Control of citrus canker and citrus bacterial spot with bacteriophages. Plant Dis 92:1048–1052Google Scholar
  11. Balogh B, Jones JB, Momol MT, Olson SM (2005) Persistence of bacteriophages as biocontrol agents in the tomato canopy. Acta Hortic 695:299–302Google Scholar
  12. Balogh B, Jones JB, Momol MT, Olson SM, Obradovic A, King P, Jackson LE (2003) Improved efficacy of newly formulated bacteriophages for management of bacterial spot on tomato. Plant Dis 87:949–954Google Scholar
  13. Basit HA, Angle JS, Salem S, Gewaily EM (1992) Phage coating of soybean seed reduces nodulation by indigenous soil bradyrhizobia. Can J Microbiol 38:1264–1269Google Scholar
  14. Berg G, Sanjaghsaz H, Wangwongwatana S (1989) Potentiation of the virucidal effectiveness of free chlorine by substances in drinking water. Appl Environ Microbiol 55:390–393PubMedGoogle Scholar
  15. Bickley J, Short SK, McDowell DG, Parkes HC (1996) Polymerase chain reaction (PCR) detection of Listeria monocytogenes in diluted milk and reversal of PCR inhibition caused by calcium ions. Lett Appl Microbiol 22:153–158PubMedGoogle Scholar
  16. Blom TJ, Brown W (1999) Preplant copper-based compounds reduce Erwinia soft rot on calla lilies. HortTechnol 9:56–59Google Scholar
  17. Borsheim KY, Bratbak G, Heldal M (1990) Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy. Appl Environ Microbiol 56:352–356PubMedGoogle Scholar
  18. Bouzari M, Emtiazi G, Mehdipour-Moghaddam MJ (2008) The effects of heavy metals and chelating agents on phage development and enumeration of Rhizobium by phage counting in different soils. Am Eurasian J Agric Environ Sci 3:420–424Google Scholar
  19. Brussaard CPD, Kempers RS, Kop A, Riegman R, Heldal M (1996) Virus-like particles in a summer bloom of Emiliana huleyi in the North Sea. Aquat Microb Ecol 10:105–113Google Scholar
  20. Brüssow H, Kutter E (2005a) Phage ecology. In: Kutter E, Sulakvelidze A (eds) Bacteriophages: biology and applications. CRC Press, Boca Raton, pp 129–163Google Scholar
  21. Brüssow H, Kutter E (2005b) Genomics and evolution of tailed phages. In: Kutter E, Sulakvelidze A (eds) Bacteriophages: biology and applications. CRC Press, Boca Raton, pp 91–128Google Scholar
  22. Burge WD, Enkiri NK (1978a) Virus adsorption by five soils. J Environ Qual 7:73–76Google Scholar
  23. Burge WD, Enkiri NK (1978b) Adsorption kinetics of bacteriophage P29103000X-174 on soil. J Environ Qual 7:536–541Google Scholar
  24. Campbell A (2006) General aspects of lysogeny. In: Calendar R (ed) The bacteriophages, 2nd edn. Oxford University Press, New YorkGoogle Scholar
  25. Campbell JIA, Albrechtsen M, Sorensen J (1995) Large Pseudomonas phages isolated from barley rhizosphere. FEMS Microbiol Ecol 18:63–74Google Scholar
  26. Canchaya C, Fournous G, Brüssow H (2004) The impact of prophages on bacterial chromosomes. Mol Microbiol 53:9–18PubMedGoogle Scholar
  27. Carlson K (2005) Working with bacteriophages: common techniques and methodological approaches. In: Kutter E, Sulakvelidze A (eds) Bacteriophages: biology and applications. CRC Press, Boca Raton, pp 437–487Google Scholar
  28. Chattopadhyay D, Chattopadhyay S, Lyon WG, Wilson JT (2002) Effect of surfactants on the survival and sorption of viruses. Environ Sci Technol 36:4017–4024PubMedGoogle Scholar
  29. Danovaro R, Dell’Anno A, Trucco A, Serresi M, Vanucci S (2001) Determination of virus abundance in marine sediments. Appl Environ Microbiol 67:1384–1387PubMedGoogle Scholar
  30. Demeke T, Adams R (1992) The effects of plant polysaccharides and buffer additives on PCR. BioTechniques 12:333–334Google Scholar
  31. Desai C, Madamwar D (2006) Extraction of inhibitor-free metagenomic DNA from polluted sediments, compatible with molecular diversity analysis using adsorption and ion-exchange treatments. Bioresour Technol 98:761–768PubMedGoogle Scholar
  32. Dowd SE, Pillai SD, SookYun W, Corapcioglu MY (1998) Delineating the specific influence of virus isoelectric point and size on virus adsorption and transport through sandy soils. Appl Environ Microbiol 64:405–410PubMedGoogle Scholar
  33. Erskine JM (1973) Characteristics of Erwinia amylovora bacteriophage and its possible role in the epidemiology of fire blight. Can J Microbiol 19:837–845PubMedGoogle Scholar
  34. Flaherty JE, Harbaugh BK, Jones JB, Somodi GC, Jackson LE (2001) H-mutant bacteriophages as a potential biocontrol of bacterial blight of geranium. HortSci 36:98–100Google Scholar
  35. Flaherty JE, Jones JB, Harbaugh BK, Somodi GC, Jackson LE (2000) Control of bacterial spot on tomato in the greenhouse and field with h-mutant bacteriophages. HortSci 35:882–884Google Scholar
  36. Foulds IV, Granacki A, Xiao C, Krull UJ, Castle AJ, Horton PJ (2002) Quantification of microcystin-producing cyanobacteria and E. coli in water by 5′-nuclease PCR. J Appl Microbiol 93:825–834PubMedGoogle Scholar
  37. Fu W, Forster T, Meyer O, Curtin JJ, Lehman SM, Donlan RM (2009) Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother. doi:10.1128/AAC.00669-09Google Scholar
  38. Germida JJ (1986) Population dynamics of Azospirillum brasilense and its bacteriophage in soil. Plant Soil 90:117–128Google Scholar
  39. Gill J, Abedon ST (2003) Bacteriophage ecology and plants. APSnet http://www.apsnet.org/online/feature/phages/ Cited: July 2009
  40. Gill JJ, Svircev AM, Smith R, Castle AJ (2003) Bacteriophages of Erwinia amylovora. Appl Environ Microbiol 69:2133–2138PubMedGoogle Scholar
  41. Goyer C (2005) Isolation and characterization of phages Stsc1 and Stsc3 infecting Streptomyces scabiei and their potential as biocontrol agents. Can J Plant Pathol 27:210–216Google Scholar
  42. Gracia-Garza JA, Blom TJ, Brown W, Roberts DP, Schneider K, Freisen M, Gombert D (2004) Increased incidence of Erwinia soft-rot on calla lilies in the presence of phosphorous. Eur J Plant Pathol 110:293–298Google Scholar
  43. Guenther S, Huwyler D, Richard S, Loessner MJ (2009) Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl Environ Microbiol 75:93–100PubMedGoogle Scholar
  44. Guzmán C, Jofre J, Blanch AR, Luana F (2007) Development of a feasible method to extract somatic coliphages from sludge, soil and treated biowaste virol Meth 144:41–48Google Scholar
  45. Guttman B, Raya R, Kutter E (2005) Basic phage biology. CRC Press, Boca Raton, FLGoogle Scholar
  46. Hagens S, Offerhaus ML (2008) Bacteriophages – new weapons for food safety. Food Technol Chicago 62:46Google Scholar
  47. Hao Y, Dick WA, Tuovinen OH (2002) PCR amplification of 16S rDNA sequences in Fe-rich sediment of coal refuse drainage. Biotechnol Lett 24:1049–1053Google Scholar
  48. Harrison MD, Franc DG, Maddox DA, Michaud JE, McCater-Zorner NJ (1987) Presence of Erwinia carotovora in surface water in North America. J Appl Bacteriol 62:565–570Google Scholar
  49. Hennes JE, Suttle CA (1995) Direct counts of viruses in natural waters and laboratory cultures by epifluorescence microscopy. Limnol Oceanogr 40:1050–1055Google Scholar
  50. Herron, PR (2004) Phage ecology and genetic exchange in soil. In: Kowalchuk GA, Bruijn, FJD, Head IM, Akkermans ADL and Elsas JDV (eds) Vol. II, Molecular microbial ecology manual, pp 1173–1183Google Scholar
  51. Hildebrand M, Tebbe CC, Geider K (2001) Survival studies with the fire blight pathogen Erwinia amylovora in soil and in a soil-inhabiting insect. J Phytopath 149:635–639Google Scholar
  52. Hu TL (1998) A comparison of two methods to recover phages from soil samples. Bioresour Technol 65:167–169Google Scholar
  53. Ibekwe AM, Watt PM, Grieve CM, Sharma VK, Lyons SR (2002) Multiplex fluorogenic real-time PCR for detection and quantification of Escherichia coli O157:H7 in dairy wastewater wetlands. Appl Environ Microbiol 68:4853–4862PubMedGoogle Scholar
  54. Iriarte FB, Balogh B, Momol MT, Smith LM, Wilson M, Jones JB (2007) Factors affecting survival of bacteriophage on tomato leaf surfaces. Appl Environ Microbiol 73:1704–1711PubMedGoogle Scholar
  55. Jensen EC, Schrader HS, Rieland B, Thompson TL, Lee KW, Nickerson KW, Kokjohn TA (1998) Prevalence of broad-host-range lytic bacteriophages of Sphaerotilus natans, Escherichia coli, and Pseudomonas aeruginosa. Appl Environ Microbiol 64:575–580PubMedGoogle Scholar
  56. Johnson KB, Stockwell VO (2000) Biological control of fire blight. In: Vanneste JL (ed) Fire blight: the disease and its causative agent, Erwinia amylovora. CaB International, Wallingford, Oxon, pp 319–337Google Scholar
  57. Jones JB, Jackson LE, Balogh B, Obradovic A, Iriarte FB, Momol MT (2007) Bacteriophages for plant disease control. Ann Rev Phytopathol 45:245–262Google Scholar
  58. Jones JB, Momol MT, Obradovic A, Balogh B, Olson SM (2005) Bacterial spot management on tomatoes. Vol. 695 Acta Hortic 119–124Google Scholar
  59. Katcher HL, Schwartz I (1994) A distinctive property of Tth DNA polymerase: enzymatic amplification in the presence of phenol. BioTechniques 16:84–92PubMedGoogle Scholar
  60. Katznelson H, Lochhead AG, Timonin MI (1948) Soil microorganisms and the rhizosphere. Bot Rev 14:543–587Google Scholar
  61. KIeczkowska J (1957) A study of the distribution and the effects of bacteriophage of root nodule bacteria in soil. Can J Microbiol 3:171–180Google Scholar
  62. Kimura M, Jia Z-J, Nakayama N, Asakawa S (2008) Ecology of viruses in soils: past, present and future perspectives. Soil Sci Plant Nut 54:1–32Google Scholar
  63. Kumar MKP, Khan ANA, Reddy CNL, Basavarajappa MP, Venkataravanappa V, Basha Z (2006) Biological control of bacterial wilt of tomato caused by Ralstonia solanacearum, race-1, biovar-III. J Plant Dis Sci 1:176–181Google Scholar
  64. Lang JM, Gent DH, Schwartz HF (2007) Management of Xanthomonas leaf blight of onion with bacteriophages and a plant activator. Plant Dis 91:871–878Google Scholar
  65. Lanning S, Williams ST (1982) Methods for the direct isolation and enumeration of actinophages in soil. J Gen Microbiol 128:2063–2071Google Scholar
  66. Lehman SM (2007) Development of a bacteriophage-based biopesticide for fire blight. PhD thesis, Brock UniversityGoogle Scholar
  67. Leroy M, Prigent MDM, Confalonieri F, Dubow M (2008) Bacteriophage morphotype and genome diversity in Seine River sediment. Freshw Biol 53:1176–1185Google Scholar
  68. Manninen A, Hall GEM, Vaive JE, MacLaurin AI (1996) Analytical aspects of the application of sodium pyrophosphate reagent in the specific extraction of the labile organic component of humus and soils. J Geochem Explor 56:23–36Google Scholar
  69. Markoishvili K, Tsitlanadze G, Katsarava R, Morris JGJ, Sulakvelidze A (2002) A novel sustained-release matrix based on biodegradable polyester amides impregnated with bacteriophages and an antibiotic shows promise in management of infected venous stasis ulcers and other poorly healing wounds. Int J Dermatol 41:453–458PubMedGoogle Scholar
  70. Marsh P, Wellington EMH (1994) Phage–host interactions in soil. FEMS Microbiol Ecol 15:99–107Google Scholar
  71. McKeague JA, Brydon JE, Miles NM (1971) Soil Sci. Soc Am Proc 35:33–38Google Scholar
  72. Mendum TA, Clark IM, Hirsch PR (2001) Characterization of two novel Rhizobium leguminosarum bacteriophages from a field release site of genetically-modified rhizobia. Antonie Van Leeuwenhoek 79:189–197PubMedGoogle Scholar
  73. Miller DN, Bryant JE, Madsen EL, Ghiorse WC (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65:4715–4724PubMedGoogle Scholar
  74. Novikova NI, Pavlova EA, Limeshchenko EV (1993) Phage sensitivity and host range of Rhizobium strains isolated from root nodules of temperate legumes. Plant Soil 151:45–53Google Scholar
  75. O’Brien RD, Lindow SE (1989) Effet of plant species and environmental conditions on epiphytic population sizes of Pseudomonas syringae and other bacteria. Phytopathology 79:619–627Google Scholar
  76. Obradovic A, Jones JB, Momol MT, Balogh B, Olson SM (2004) Management of tomato bacterial spot in the field by foliar applications of bacteriophages and SAR inducers. Plant Dis 88:736–740Google Scholar
  77. Obradovic A, Jones JB, Momol MT, Olson SM, Jackson LE, Balogh B, Guven K, Iriarte FB (2005) Integration of biological control agents and systemic acquired resistance inducers against bacterial spot on tomato. Plant Dis 89:712–716Google Scholar
  78. Ogram A (1998) Isolation of nucleic acids from environmental samples. In: Burlage RS, Atlas R, Stahl D, Geesey G, Sayler G (eds) Techniques in microbial ecology. Oxford University Press, Oxford UK, pp 273–288Google Scholar
  79. Pantastico-Caldas M, Duncan KE, Istock CA, Bell JA (1992) Population dynamics of bacteriophage and Bacillus subtilis in soil. Ecology 73:1888–1902Google Scholar
  80. Pérombelon MCM, Kelmon A (1980) Ecology of the soft rot Erwinias. Ann Rev Phytopathol 18:361–387Google Scholar
  81. Ravensdale M, Blom TJ, Gracia Garza JA, Svircev AM, Smith RJ (2007) Bacteriophages and the control of Erwinia carotovora subsp. carotovora. Can J Plant Pathol 29:121–130Google Scholar
  82. Ritchie DF (1978) Bacteriophages of Erwinia amyovora: Their isolation, distribution, characterization, and possible involvement in the etiology and epidemiology of fire blight. PhD thesis, Michigan State UniversityGoogle Scholar
  83. Ritchie DF, Klos EJ (1977) Isolation of Erwinia amyolovora bacteriophage from aerial parts of apple trees. Phytopathology 67:101–104Google Scholar
  84. Ritchie DF, Klos EJ (1979) Some properties of Erwinia amylovora bacteriophages. Phytopathology 69:1078–1083Google Scholar
  85. Romeo AM, Christen L, Niles EG, Kosman DJ (2001) Intracellular chelation of iron by bipyridyl inhibits DNA virus replication. J Biol Chem 24:301–308Google Scholar
  86. Saccardi A, Gambin E, Zaccardelli M, Barone G, Mazzucchi U (1993) Xanthomonas campestris pv. pruni control trials with phage treatments on peach in the orchard. Phytopathol Mediterr 32:206–210Google Scholar
  87. Sagripanti J-L (1992) Metal-based formulations with high microbiocidal activity. Appl Environ Microbiol 58:3157–3162PubMedGoogle Scholar
  88. Sander M, Schmieger H (2001) Method for host-independent detection of generalized transducing bacteriophages in natural habitats. Appl Environ Microbiol 67:1490–1493PubMedGoogle Scholar
  89. Satsangi J, Jewell DP, Welsh K, Bunce M, Bell JI (1994) Effect of heparin on polymerase chain reaction. Lancet 343:1509–1510PubMedGoogle Scholar
  90. Schnabel EL, Fernando WGD, Meyer MP, Jones AL, Jackson LE (1999) Bacteriophage of Erwinia amylovora and their potential for biocontrol. Acta Hortic 489:649–653Google Scholar
  91. Schnabel EL, Jones AL (2001) Isolation and characterization of five Erwinia amylovora bacteriophages and assessment of phage resistance in strains of Erwinia amylovora. Appl Environ Microbiol 67:59–64PubMedGoogle Scholar
  92. Sillankorva S, Oliveira R, Viera MJ, Sutherland I, Azeredo J (2006) Pseudomonas fluorescens infection by bacteriophage øS1: the influence of temperature, host growth phase and media. FEMS Microbiol Lett 241:13–20Google Scholar
  93. Sjöstedt A, Eriksson U, Ramisse V, Garrigue H (1997) Detection of Bacillus anthracis spores in soil by PCR. FEMS Microbiol Ecol 23:159–168Google Scholar
  94. Smit E, Wolters AC, Lee H, Trevors JT, van Elsas JD (1996) Interactions between a genetically marked Pseudomonas fluorescens strain and bacteriophage FR2f in soil: effects of nutrients, alginate encapsulation, and the wheat rhizosphere. Microb Ecol 31:125–140Google Scholar
  95. 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 159:349–357PubMedGoogle Scholar
  96. Stephens PM, O’Sullivan M, Gara F (1987) Effect of bacteriophages on colonization of sugar beet roots by Pseudomonas spp. Appl Environ Microbiol 53:1164–1167Google Scholar
  97. Stewart A (2001) Commercial biocontrol – reality or fantasy? Australas. Plant Pathol 30:127–131Google Scholar
  98. Suslow TV (1986) Bacteriophage-resistant plant growth promoting rhizobactria. USA Patent 4584274Google Scholar
  99. Svircev AM, Gill JJ, Sholberg P (2002a) Erwinia amylovora (Burrill) Winslow, Broadhurst, Buchanan, Krumwiede, Rogers and Smith, fire blight (Enterobacteriaceae). In: Mason PG, Huber JT (eds) Biological control programmes in Canada. CaBI Publishing, Wallingford UK, pp 448–451Google Scholar
  100. Svircev AM, Lehman SM, Kim W-S, Barszcz E, Schneider KE, Castle AJ (2006) Control of the fire blight pathogen with bacteriophages. In: Proceedings of the 1st International Symposium on Biological control of Bacterial Plant Diseases. Zeller W and Ullrich C (eds) Arno Brynda, Berlin Germany, pp 259–261Google Scholar
  101. Svircev AM, Smith R, Gracia-Garza JA, Gill JJ, Schneider K (2002b) Biocontrol of Erwinia with bacteriophages. Bull OILB/SROP 25:10, p. 139–142Google Scholar
  102. 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 155:51–60Google Scholar
  103. Sykes IK, Lanning S, St W (1981) The effect of pH on soil actinophage. Microbiol 122:271–280Google Scholar
  104. Tan JSH, Reanney DC (1976) Interactions between bacteriophages and bacteria in soil. Soil Biol Biochem 8:145–150Google Scholar
  105. Taylor DH, Moore RS, Sturman LS (1981) Influence of pH and electrolyte composition on adsorption of poliovirus by soils and minerals. Appl Environ Microbiol 42:976–984PubMedGoogle Scholar
  106. Torsvik V, Goksřyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787PubMedGoogle Scholar
  107. Tsai YL, Olsen B (1992) Rapid method for separation of bacterial DNA from humic substances in sediments for polymerase chain reaction. Appl Environ Microbiol 58:2292–2295PubMedGoogle Scholar
  108. Vanneste JL (ed) (2000) Fire blight: the disease and its causative agent, Erwinia amylovora. CaB International, Wallingford, UKGoogle Scholar
  109. Van Twest R, Kropinski AM (2009) Bacteriophage enrichment from water and soil. In: Clokie MRJ, Kropinski AM (eds) Bacteriophages, methods and protocols, Vol. 1: Isolation, characterization and interactions. Methods in molecular biology, Walker JM (series ed). Humana Press part of Springer Science + Business Media, Totowa, NJGoogle Scholar
  110. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181PubMedGoogle Scholar
  111. Weinbauer MG, Suttle CA (1997) Comparison of epifluorescence and transmission electron microscopy for counting viruses in natural marine waters. Aquat Microb Ecol 13:225–232Google Scholar
  112. Wiedbrauk DL, Werner JC, Drevon AM (1995) Inhibition of PCR by aqueous and vitreous fluids. J Clin Microbiol 33:2643–2646PubMedGoogle Scholar
  113. Wiggins BA, Alexander M (1985) Minimum bacterial density for bacteriophage replication: implications for significance of bacteriophages in natural ecosystems. Appl Environ Microbiol 49:19–23PubMedGoogle Scholar
  114. Williamson KE, Radosevich M, Wommack KE (2005) Abundance and diversity of viruses in six Delaware soils. Appl Environ Microbiol 71:3119–3125PubMedGoogle Scholar
  115. Williamson KE, Wommack KE, Radosevich M (2003) Sampling natural viral communities from soil for culture-independent analyses. Appl Environ Microbiol 69:6628–6633PubMedGoogle Scholar
  116. Wilson IG (1997) Inhibition and facilitation of nucleic acid amplification. Appl Environ Microbiol 63:3741–3751PubMedGoogle Scholar
  117. Yamada T, Kawasaki T, Nagata S, Fujiwara A, Usami S, Fujie M (2007) New bacteriophages that infect the phytopathogen Ralstonia solanacearum. Microbiology 153:2630–2639PubMedGoogle Scholar
  118. Young CC, Burghoff RL, Keim LG, Minak-Bernero V, Lute JR, Hinton SM (1993) Polyvinylpyrrolidone-agarose gel electrophoresis purification of polymerase chain reaction-amplifiable DNA from soils. Appl Environ Microbiol 59:1971–1974Google Scholar
  119. Zaccardelli M, Saccardi A, Gambin E, Mazzucchi U (1992) Xanthomonas campestris pv. pruni bacteriophages on peach trees and their potential use for biological control. Phytopathol mediterr 31:133–140Google Scholar
  120. Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322PubMedGoogle Scholar
  121. Zipper H, Buta C, Lämmle K, Brunner H, Bernhagen J, Vitzthum F (2003) Mechanisms underlying the impact of humic acids on DNA quantification by SYBR Green I and consequences for the analysis of soils and aquatic sediments. Nucleic Acids Res 31:e39PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Antonet M. Svircev
    • 1
  • Susan M. Lehman
    • 2
  • Peter Sholberg
    • 3
  • Dwayne Roach
    • 4
  • Alan J. Castle
    • 4
  1. 1.Agriculture and Agri-FoodVineland StationCanada
  2. 2.Division of Healthcare Quality PromotionCenters for Disease Control and PreventionAtlantaUSA
  3. 3.Agriculture and Agri-Food Canada, Pacific Agri-Food Research CentreSummerlandCanada
  4. 4.Department of Biological ScienceBrock UniversitySt. CatharinesCanada

Personalised recommendations