F+RNA coliphage typing for microbial source tracking in surface waters

Journal of Applied Microbiology

Volumn 101, Issue 5, 2006, Pages 1015-1026

  Stewart Pullaro, J ^a,b   Daugomah, J W ^a   Chestnut, D E ^c   Graves, D A ^c   Sobsey, M D ^b   Scott, G I ^a  

^a CENTER FOR COASTAL ENVIRONMENTAL HEALTH AND BIOMOLECULAR RESEARCH   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c Bureau of Water SC Dept of Health Envtl Control   (United States)

Author keywords

Coliforms; Coliphages; Faecal contamination; Microbial source tracking; Water quality

Indexed keywords

CONTAMINATION; ESCHERICHIA COLI; RIVER POLLUTION; RNA; SURFACE DISCHARGES; VIRUSES; WATER QUALITY;

COLIFORMS; COLIPHAGES; FECAL COLIFORM; FECAL CONTAMINATION; FECAL POLLUTION; MICROBIAL SOURCE TRACKING; PRESENCE-ABSENCE; SOMATIC COLIPHAGES; SOUTH CAROLINA; WATER SAMPLES;

SURFACE WATERS;

SURFACE WATER; VIRUS RNA;

BIOMONITORING; FECAL COLIFORM; IDENTIFICATION METHOD; POLLUTANT SOURCE; STANDARD (REGULATION); SURFACE WATER; WATER POLLUTION; WATER QUALITY;

ARTICLE; BACTERIUM CONTAMINATION; COLIPHAGE; ESCHERICHIA COLI; FECES MICROFLORA; NONHUMAN; VIRUS ISOLATION; VIRUS TYPING; WASTE WATER; WATER CONTAMINATION; WATER QUALITY;

NORTH AMERICA; SOUTH CAROLINA; UNITED STATES;

ANIMALIA; ESCHERICHIA COLI;

EID: 33750057648     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2006.03011.x     Document Type: Article

References (68)

1. APHA (1995) Standard Methods for the Examination of Water and Wastewater. Washington, DC, USA: American Public Health Association.
2. Armon, R. and Kott, Y. (1996) Bacteriophages as indicators of pollution. Crit Rev Environ Sci Technol 26, 299-335.
3. Beekwilder, J., Nieuwenhuizen, R., Havelaar, A.H. and van Duin, J. (1996) An oligonucleotide hybridization assay for the identification and enumeration of F-specific RNA phages in surface water. J Appl Bacteriol 80, 179-186.
4. Bernhard, A.E., Goyard, T., Simonich, M.T. and Field, K.G. (2003) Application of a rapid method for identifying fecal pollution sources in a multi-use estuary. Water Res 37, 909-913.
5. Borrego, J.J., Morinigo, M.A., Vincente, A., Cornax, R. and Romero, P. (1987) Coliphages as an indicator of fecal pollution in water - its relationship with indicator and pathogenic microorganisms. Water Res 21, 1473-1480.
6. Brion, G.M., Meschke, J.S. and Sobsey, M.D. (2002) F-specific RNA coliphages: occurrence, types, and survival in natural waters. Water Res 36, 2419-2425.
7. Calci, K.R., Burkhardt, W. III, Watkins, W.D. and Rippey, S.R. (1998) Occurrence of male-specific bacteriophage in feral and domestic animal wastes, human feces, and human-associated wastewaters. Appl Environ Microbiol 64, 5027-5029.
8. Carson, C.A., Shear, B.L., Ellersieck, M.R. and Asfaw, A. (2001) Identification of fecal Escherichia coli from humans and animals by ribotyping. Appl Environ Microbiol 67, 1503-1507.
9. Carson, C.A., Shear, B.L., Ellersieck, M.R. and Schnell, J.D. (2003) Comparison of ribotyping and repetitive extragenic palindromic-PCR for identification of fecal Escherichia coli from humans and animals. Appl Environ Microbiol 69, 1836-1839.
10. Cole, D., Long, S.C. and Sobsey, M.D. (2003) Evaluation of F+ RNA and DNA coliphages as source-specific indicators of fecal contamination in surface waters. Appl Environ Microbiol 69, 6507-6514.
11. Cornax, R., Morinigo, M.A., Balebona, M.C., Castro, D. and Borrego, J.J. (1991) Significance of several bacteriophage groups as indicators of sewage pollution in marine waters. Water Res 25, 675-678.
12. Cornax, R., Morinigo, M.A., Gonzalez-Jaen, F., Alonso, M.C. and Borrego, J.J. (1994) Bacteriophages presence in human faeces of healthy subjects and patients with gastrointestinal disturbances. Zentralbl Bakteriol 281, 214-224.
13. Dhillon, E.K. and Dhillon, T.S. (1974) Synthesis of indicator strains and density of ribonucleic acid-containing coliphages in sewage. Appl Microbiol 27, 640-647.
14. Dombek, P.E., Johnson, L.K., Zimmerley, S.T. and Sadowsky, M.J. (2000) Use of repetitive DNA sequences and the PCR To differentiate Escherichia coli isolates from human and animal sources. Appl Environ Microbiol 66, 2572-2577.
15. Doré, W.J., Henshilwood, K. and Lees, D.N. (2000) Evaluation of F-specific RNA bacteriophage as a candidate human enteric virus indicator for bivalve molluscan shellfish. Appl Environ Microbiol 66, 1280-1285.
16. Duran, M., Haznedarog¢lu, B.Z. and Zitomer, D.H. (2006) Microbial source tracking using host specific FAME profiles of fecal coliforms. Water Res 40, 67-74.
17. EPA (2001a) Method 1602. Male-specific (F+) and Somatic Coliphage in Water by Single Agar Layer (SAL) Procedure. Washington, DC, USA: EPA Office of Water.
18. EPA (2001b) Method 1601. Male-specific (F+) and Somatic Coliphage in Water by Two-step Enrichment Procedure. Washington, DC, USA: EPA Office of Water.
19. Field, K.G., Chern, E.C., Dick, L.K., Fuhrman, J., Griffith, J., Holden, P.A., LaMontagne, M.G., Olson, B. et al. (2003) A comparative study of culture-independent, library-independent genotypic methods of fecal source tracking. J Water Health 1, 181-194.
20. Fong, T.T., Griffin, D.W. and Lipp, E.K. (2005) Molecular assays for targeting human and bovine enteric viruses in coastal waters and their application for library-independent source tracking. Appl Environ Microbiol 71, 2070-2078.
21. Furuse, K. (1987) Distribution of coliphages in the environment: general considerations. In Phage Ecology ed. Goyal, S.M., Gerba, C.P. and Bitton, G. pp. 87-124. New York, USA: John Wiley & Sons.
22. Furuse, K., Ando, A. and Watanabe, I. (1975) Isolation and grouping of RNA phages: V. A survey in the islands in the adjacent seas of Japan. J Keio Med Soc 52, 259-263.
23. Gantzer, C., Maul, A., Audic, J.M. and Schwartzbrod, L. (1998) Detection of infectious enteroviruses, enterovirus genomes, somatic coliphages, and Bacteroides fragilis phages in treated wastewater. Appl Environ Microbiol 64, 4307-4312.
24. Geldreich, E.E. and Kenner, B.A. (1969) Concepts of fecal streptococci in stream pollution. J Water Pollut Control Fed 41 (Suppl.), R336-352.
25. Griffin, D.W., Stokes, R., Rose, J.B. and Paul, J.H. III (2000) Bacterial indicator occurrence and the use of an F(+) specific RNA coliphage assay to identify fecal sources in Homosassa Springs, Florida. Microb Ecol 39, 56-64.
26. Hagedorn, C., Robinson, S.L., Filtz, J.R., Grubbs, S.M., Angier, T.A. and Reneau, R.B. (1999) Determining sources of fecal pollution in a rural Virginia watershed with antibiotic resistance patterns in fecal streptococci. Appl Environ Microbiol 65, 5522-5531.
27. Hagedorn, C., Crozier, J.B., Mentz, K.A., Booth, A.M., Graves, A.K., Nelson, N.J. and Reneau, R.B. (2003) Carbon source utilization profiles as a method to identify sources of faecal pollution in water. J Appl Microbiol 94, 792-799.
28. Harwood, V.J., Whitlock, J. and Withington, V. (2000) Classification of antibiotic resistance patterns of indicator bacteria by discriminant analysis: use in predicting the source of fecal contamination in subtropical waters. Appl Environ Microbiol 66, 3698-3704.
29. Havelaar, A.H. (1993) Bacteriophages as models of human enteric viruses in the environment. ASM News 59, 614-619.
30. Havelaar, A.H., Furuse, K. and Hogeboom, W.M. (1986) Bacteriophages and indicator bacteria in human and animal faeces. J Appl Bacteriol 60, 255-262.
31. Havelaar, A.H., Pot-Hogeboom, W.M., Furuse, K., Pot, R. and Hormann, M.P. (1990) F-specific RNA bacteriophages and sensitive host strains in faeces and wastewater of human and animal origin. J Appl Bacteriol 69, 30-37.
32. Hsu, F.C., Shieh, Y.S., van Duin, J., Beekwilder, M.J. and Sobsey, M.D. (1995) Genotyping male-specific RNA coliphages by hybridization with oligonucleotide probes. Appl Environ Microbiol 61, 3960-3966.
33. Hsu, F.-C., Handzel, T.R., Lovelace, G., Stewart, J.R., Sobsey, M.D., Thompson, S.S. and Yates, M.V. (1998) Improved Methods to Detect low levels of Coliphages in Water by Enrichment Presence-Absence and Membrane Filter Methods. 1998 Water Quality Technology Conference. Denver, CO: American Water Works Association.
34. IAWPRC (1991) Bacteriophages as model viruses in water quality control. Water Res 25, 529-545.
35. Jiang, S., Noble, R. and Chu, W. (2001) Human adenoviruses and coliphages in urban runoff-impacted coastal waters of southern California. Appl Environ Microbiol 67, 179-184.
36. Jimenez-Clavero, M.A., Fernandez, C., Ortiz, J.A., Pro, J., Carbonell, G., Tarazona, J.V., Roblas, N. and Ley, V. (2003) Teschoviruses as indicators of porcine fecal contamination of surface water. Appl Environ Microbiol 69, 6311-6315.
37. Johnson, L.K., Brown, M.B., Carruthers, E.A., Ferguson, J.A., Dombek, P.E. and Sadowsky, M.J. (2004) Sample size, library composition, and genotypic diversity among natural populations of Escherichia coli from different animals influence accuracy of determining sources of fecal pollution. Appl Environ Microbiol 70, 4478-4485.
38. Khatib, L.A., Tsai, Y.L. and Olson, B.H. (2002) A biomarker for the identification of cattle fecal pollution in water using the LTIIa toxin gene from enterotoxigenic Escherichia coli. Appl Microbiol Biotechnol 59, 97-104.
39. Khatib, L.A., Tsai, Y.L. and Olson, B.H. (2003) A biomarker for the identification of swine fecal pollution in water, using the STII toxin gene from enterotoxigenic Escherichia coli. Appl Microbiol Biotechnol 63, 231-238.
40. Kott, Y., Rose, J., Sperber, S. and Betzer, N. (1974) Bacteriophages as viral pollution indicators. Water Res 8, 165-171.
41. Lewis, G.D., Loutit, M.W. and Austin, F.J. (1985) A method for detecting human enteroviruses in aquatic sediments. J Virol Methods 10, 153-162.
42. Ley, V., Higgins, J. and Fayer, R. (2002) Bovine enteroviruses as indicators of fecal contamination. Appl Environ Microbiol 68, 3455-3461.
43. Long, S.C., Arango, P.C. and Plummer, J.D. (2005a) An optimized enumeration method for sorbitol-fermenting Bifidobacteria in water samples. Can J Microbiol 51, 413-422.
44. Long, S.C., El-Khoury, S.S., Oudejans, D.J.G., Sobsey, M.D. and Vinjé, J. (2005b) Assessment of sources and diversity of male-specific coliphages for source tracking. Environ Eng Sci 22, 367-377.
45. Maluquer de Motes, C., Clemente-Casares, P., Hundesa, A., Martin, M. and Girones, R. (2004) Detection of bovine and porcine adenoviruses for tracing the source of fecal contamination. Appl Environ Microbiol 70, 1448-1454.
46. Mara, D.D. and Oragui, J.I. (1981) Occurrence of Rhodococcus coprophilus and associated actinomycetes in feces, sewage, and freshwater. Appl Environ Microbiol 42, 1037-1042.
47. Meschke, J.S. and Sobsey, M.D. (2003) Comparative reduction of Norwalk virus, poliovirus type 1, F+ RNA coliphage MS2 and Escherichia coli in miniature soil columns. Water Sci Technol 47, 85-90.
48. Moore, D.F., Harwood, V.J., Ferguson, D.M., Lukasik, J., Hannah, P., Getrich, M. and Brownell, M. (2005) Evaluation of antibiotic resistance analysis and ribotyping for identification of faecal pollution sources in an urban watershed. J Appl Microbiol 99, 618-628.
49. Morinigo, M.A. (1992) Evaluation of different bacteriophage groups as fecal indicators in contaminated natural waters in southern England. Water Res 26, 267-271.
50. Muniesa, M., Moce-Llivina, L., Katayama, H. and Jofre, J. (2003) Bacterial host strains that support replication of somatic coliphages. Antonie Van Leeuwenhoek 83, 305-315.
51. Nebra, Y., Bonjoch, X. and Blanch, A.R. (2003) Use of Bifidobacterium dentium as an indicator of the origin of fecal water pollution. Appl Environ Microbiol 69, 2651-2656.
52. Noble, R.T. and Fuhrman, J.A. (2001) Enteroviruses detected by reverse transcriptase polymerase chain reaction from the coastal waters of Santa Monica Bay, California: low correlation to bacterial indicators. Hydrobiologia 460, 175-184.
53. Parveen, S., Murphree, R.L., Edmiston, L., Kaspar, C.W., Portier, K.M. and Tamplin, M.L. (1997) Association of multiple-antibiotic-resistance profiles with point and nonpoint sources of Escherichia coli in Apalachicola Bay. Appl Environ Microbiol 63, 2607-2612.
54. Parveen, S., Portier, K.M., Robinson, K., Edmiston, L. and Tamplin, M.L. (1999) Discriminant analysis of ribotype profiles of Escherichia coli for differentiating human and nonhuman sources of fecal pollution. Appl Environ Microbiol 65, 3142-3147.
55. Payment, P. and Hunter, P.R. (2001) Endemic and epidemic infectious intestinal disease and its relationship to drinking water. In Water Quality: Guidelines, Standards and Health. Assessment of Risk and Risk Management for Water-related Infectious Disease ed. Fewtrell, L. and Bartram, J. London, UK: IWA Publishing, on behalf of the World Health Organization.
56. Schaper, M., Jofre, J., Uys, M. and Grabow, W.O. (2002a) Distribution of genotypes of F-specific RNA bacteriophages in human and non-human sources of faecal pollution in South Africa and Spain. J Appl Microbiol 92, 657-667.
57. Schaper, M., Duran, A.E. and Jofre, J. (2002b) Comparative resistance of phage isolates of four genotypes of F-specific RNA bacteriophages to various inactivation processes. Appl Environ Microbiol 68, 3702-3707.
58. Scott, T.M., Parveen, S., Portier, K.M., Rose, J.B., Tamplin, M.L., Farrah, S.R., Koo, A. and Lukasik, J. (2003) Geographical variation in ribotype profiles of Escherichia coli isolates from humans, swine, poultry, beef, and dairy cattle in Florida. Appl Environ Microbiol 69, 1089-1092.
59. Scott, T.M., Jenkins, T.M., Lukasik, J. and Rose, J.B. (2005) Potential use of a host associated molecular marker in Enterococcus faecium as an index of human fecal pollution. Environ Sci Technol 39, 283-287.
60. Seeley, N.D. and Primrose, S.B. (1980) The effect of temperature on the ecology of aquatic bacteriophages. J Gen Virol 46, 87-95.
61. Simmons, G.M., Waye, D.F., Herbein, S., Myers, S. and Walker, E. (2000) Estimating nonpoint fecal coliform sources in northern Virginia's Four Mile Run watershed. In Virginia Water Research Symposium Special Report SR-19-2000 ed. Younos, T. and Poff, J. pp. 248-267. Blacksburg, VA, USA: Virginia Water Resources Research Centre.
62. Stewart, J.R., Vinjé, J., Oudejans, S., Scott, G. and Sobsey, M.D. (2006) Sequence variation among group III F-specific RNA coliphages from water samples and swine lagoons. Appl Environ Microbiol 72, 1226-1230.
63. Ufnar, J.A., Wang, S.Y., Christiansen, J.M., Yampara-Iquise, H., Carson, C.A. and Ellender, R.D. (2006) Detection of the nifH gene of Methanobrevibacter smithii: A potential tool to identify sewage pollution in recreational waters. J Appl Microbiol 101, 44-52.
64. Wheeler, A.L., Hartel, P.G., Godfrey, D.G., Hill, J.L. and Segars, W.I. (2002) Potential of Enterococcus faecalis as a human fecal indicator for microbial source tracking. J Environ Qual 31, 1286-1293.
65. Wiggins, B.A. and Alexander, M. (1985) Minimum bacterial density for bacteriophage replication: implications for significance of bacteriophages in natural ecosystems. Appl Environ Microbiol 49, 19-23.
66. Wiggins, B.A., Andrews, R.W., Conway, R.A., Corr, C.L., Dobratz, E.J., Dougherty, D.P., Eppard, J.R., Knupp, S.R. et al. (1999) Use of antibiotic resistance analysis to identify nonpoint sources of fecal pollution. Appl Environ Microbiol 65, 3483-3486.
67. Wiggins, B.A., Cash, P.W., Creamer, W.S., Dart, S.E., Garcia, P.P., Gerecke, T.M., Han, J., Henry, B.L. et al. (2003) Use of antibiotic resistance analysis for representativeness testing of multiwatershed libraries. Appl Environ Microbiol 69, 3399-3405.
68. Woody, M.A. and Cliver, D.O. (1997) Replication of coliphage Q beta as affected by host cell number, nutrition, competition from insusceptible cells and non-FRNA coliphages. J Appl Microbiol 82, 431-440.