Estimation of pig fecal contamination in a river catchment by real-time PCR using two Pig-Specific Bacteroidales 16S rRNA genetic markers

Applied and Environmental Microbiology

Volumn 75, Issue 10, 2009, Pages 3045-3054

  Mieszkin, Sophie ^a   Furet, Jean Pierre ^b   Corthier, Gérard ^b   Gourmelon, Michèle ^a  

^a IFREMER   (France)

^b CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA; 16S RRNA GENE; CLONE LIBRARY; ENVIRONMENTAL WATER SAMPLES; FECAL CONTAMINATION; FECAL POLLUTION; GENETIC MARKERS; MICROBIAL SOURCE TRACKING METHODS; MICROBIOLOGICAL QUALITY; REAL-TIME PCR; RIVER CATCHMENT; RIVER WATER; RIVER WATER SAMPLES; SLURRY TREATMENT; WATER SAMPLES;

CATCHMENTS; CLONING; CONCENTRATION (PROCESS); CONTAMINATION; FARMS; POLLUTION DETECTION; RANGE FINDING; RIVERS; RUNOFF;

RIVER POLLUTION;

RIVER WATER; RNA 16S;

BIOMARKER; CATCHMENT; CONCENTRATION (COMPOSITION); GENETIC ANALYSIS; MICROBIOLOGY; POLYMERASE CHAIN REACTION; RNA; RUMINANT; WATER QUALITY;

ARTICLE; BACTERIAL GENE; BACTEROIDALES; CONTROLLED STUDY; COW; FECES; FRANCE; GENE LIBRARY; GENETIC MARKER; HORSE; HUMAN; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PIG FARMING; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SWINE; WATER CONTAMINATION; WATER SAMPLING;

ANIMALS; BACTEROIDETES; CATTLE; CLUSTER ANALYSIS; DNA PRIMERS; DNA, BACTERIAL; DNA, RIBOSOMAL; FRANCE; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; RIVERS; RNA, RIBOSOMAL, 16S; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SWINE; WATER POLLUTION;

ANIMALIA; BACTEROIDALES; BOS; BOVINAE; SUIDAE;

EID: 66249125965     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02343-08     Document Type: Article

References (56)

1. Anonymous. 1991. Detection and enumeration of Escherichia coli and coli- form bacteria in surface and waste water. Miniaturized method (most probable number) by inoculation in liquid medium. NF EN ISO 9308-3: water quality. International Organization for Standardization, Geneva, Switzerland.
2. Ashelford, K. E., N. A. Chuzhanova, J. C. Fry, A. J. Jones, and A. J. Weightman. 2006. New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl. Environ. Microbiol. 72:5734-5741.
3. Baudart, J. J., J. Gradulos, J. P. Barusseau, and P. Lebaron. 2000. Salmonella spp. and fecal coliform loads in coastal waters from a point vs. nonpoint source of pollution. J. Environ. Qual. 29:241-250.
4. Bernet, N., J. P. Delgenes, and R. Moletta. 2000. Pig slurry: the biological solution. Biofutur 197:42-45. (In French.)
5. Bernhard, A. E., and K. G. Field. 2000. Identification of nonpoint sources of fecal pollution in coastal waters by using host-specific 16S ribosomal DNA genetic markers from fecal anaerobes. Appl. Environ. Microbiol. 66:1587-1594.
6. Brown, P. E., O. F. Christensen, H. E. Clough, P. J. Diggle, C. A. Hart, S. Hazel, R. Kemp, A. J. H. Leatherbarrow, A. Moore, J. Sutherst, J. Turner, N. J. Williams, E. J. Wright, and N. P. French. 2004. Frequency and special distribution of environmental Campylobacter spp. Appl. Environ. Microbiol. 70:6501-6511.
7. Cools, D., R. Merckx, K. Vlassak, and J. Verhaegen. 2001. Survival of E. coli and Enterococcus spp. derived from pig slurry in soils of different texture. Appl. Soil Ecol. 17:53-62.
8. Cox, P., M. Griffith, M. Angles, D. Deere, and C. Ferguson. 2005. Concentration of pathogens and indicators in animal feces in the Sydney watershed. Appl. Environ. Microbiol. 71:5929-5934.
9. Dick, L. K., and K. G. Field. 2004. Rapid estimation of numbers of fecal Bacteroidales by use of a quantitative PCR assay for 16S rRNA genes. Appl. Environ. Microbiol. 70:5695-5697.
10. Dick, L. K., A. E. Bernhard, T. J. Brodeur, J. W. Santo Domingo, J. M. Simpson, S. P. Walters, and K. G. Field. 2005. Host distributions of uncultivated fecal Bacteroidales bacteria reveal genetic markers for fecal source identification. Appl. Environ. Microbiol. 71:3184-3191.
11. Edberg, S. C., E. W. Rice, R. J. Karling, and M. J. Allen. 2000. Escherichia coli: the best biological drinking water indicator for public health protection. J. Appl. Microbiol. 88:105S-116S.
12. Eurostat. 2003. Pig stock trends in European Union, 1994-2002. Eurostat, Luxembourg. http://www.eds-destatis.de/en/downloads/sif/nn-03-36.pdf.
13. Feldhusen, F. 2000. The role of seafood in bacterial foodborne diseases. Microbes Infect. 2:1651-1660.
14. Fisher, L. D., and G. Belle. 1993. Biostatistics: a methodology for health sciences. Wiley, New York, NY.
15. Galtier, N., M. Gouy, and C. Gautier. 1996. SEAVIEW and PHYLO-WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12:543-548.
16. Geldreich, E. E. 1978. Bacterial populations and indicator concepts in feces, sewage, stormwater and solid wastes, p. 51-97. In G. Berg (ed.), Indicators of viruses in water and food. Arbor Science, Ann Arbor, MI.
17. Gessel, P. D., H. C. Neil, G. M. Sagar, J. J. Lee, and J. Webb. 2004. Persistence of zoonotic pathogens in surface soil treated with different rates of liquid pig manure. Appl. Soil Ecol. 24:237-243.
18. Godfree, A., and J. Farell. 2005. Processes for managing pathogens. J. Environ. Qual. 34:105-113.
19. Gourmelon, M., M. P. Montet, S. Lozach, C. Le Mennec, M. Pommepuy, L. Beutin, and C. Vernozy-Rozand. 2006. First isolation of Shiga toxin 1d producing Escherichia coli variant strains in shellfish from coastal areas in France. J. Appl. Microbiol. 100:85-97.
20. Gourmelon, M., M. P. Caprais, R Segura, C. Le Mennec, S. Lozach, J. Y. Piriou, and A. Rince. 2007. Evaluation of two library-independent microbial source tracking methods to identify sources of fecal contamination in French estuaries. Appl. Environ. Microbiol. 73:4857-4866.
21. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
22. Hancock, D., T. Besser, J. Lejeunes, M. Davis, and D. Rice. 2001. The control of VTEC in the animal reservoir. Int. J. Food Microbiol. 66:71-78.
23. Handler, N. B., A. Paytan, C. P. Higgens, R. G. Luthy, and A. B. Boehm. 2006. Human development is linked to multiple water-body impairments along the California Coast. Estuaries Coasts 29:860-870.
24. Ibekwe, A. M., M. W. Pamela, M. G. Catherine, K. S. Vijay, and R. L. Steven. 2002. Multiplex fluorogenic real-time PCR for detection and quantification of Escherichia coli O157:H7 in dairy wastewater wetlands. Appl. Environ. Microbiol. 68:4853-4862.
25. Kildare, B. J., C. M. Leutenegger, B. S. McSwain, D. G. Bambic, V. B. Rajal, and S. Wuertz. 2007. 16S rRNA-based assays for quantitative detection of universal, human-, cow-, and dog-specific fecal Bacteroidales: a Bayesian approach. Water Res. 41:3701-3715.
26. Kimura, M. 1980. A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
27. Klappenbach, J. A., P. R. Saxman, J. R. Cole, and T. M. Schmidt. 2001. rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res. 29:181-184.
28. Koopmans, M., and E. Duizer. 2004. Foodborne viruses: an emerging problem. Int. J. Food Microbiol. 90:23-41.
29. Layton, A., L. McKay, D. Williams, V. Garrett, R. Gentry, and G. Sayler. 2006. Development of Bacteroides 16S rRNA gene TaqMan-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water. Appl. Environ. Microbiol. 72:4214-4224.
30. Legrand, L., J. Tap, C. Gauthey, J. Dore, C. Caron, and M. Leclerc. 2008. RapidOTU: a fast pipeline to analyse 16S rDNA sequences by alignment or tetranucleotide frequency. Proc. Gut Microbiome Symp. 2008 6th Congr. INRA Rowett Res. Inst., poster 26, p. 35.
31. Leung, K., and E. Topp. 2001. Bacterialcommunitydynamics inliquid swine manure during storage: molecular analysis using DGGE/PCR of 16S rDNA. FEMS Microbiol. Ecol. 38:169-177.
32. Levasseur, P., and N. Lemaire. 2003. The situation of pig slurry treatment in France. Techni-Porc 26:41-42. (In French.)
33. Lipp, E. K., and J. B. Rose. 1997. The role of seafood in foodborne diseases in the United States of America. Rev. Sci. Tech. 16:620-640.
34. Mara, D. D., and J. I. Oragui. 1983. Sorbitol- fermenting bifidobacteria as specific indicators of human faecal pollution. J. Appl. Bacteriol. 55:349-357.
35. Mawdsley, J. L., R. D. Bardgett, R. J. Merry, B. F. Pain, and M. K. Theo- dorou. 1995. Pathogens in livestock waste, their potential for movement through soil and environmental pollution. Appl. Soil Ecol. 2:1-15.
36. National Agricultural Statistics Service. 2002. Monthly hogs and pigs. National Agricultural Statistics Service, U.S. Department of Agriculture, Washington, DC. www.nass.usda.gov/.
37. Okabe, S., N. Okayama, O. Savichtcheva, and T. Ito. 2007. Quantification of host-specific Bacteroides-Prevotetta 16S rRNA genetic markers for assessment of fecal pollution in freshwater. Appl. Microbiol. Biotechnol. 74:890-901.
38. Peu, P., H. Brugère, A. M. Pourcher, M. Kérouré dan, J. J. Godon, J. J. Delgenès, and P. Dabert. 2006. Dynamics of a pig slurry microbial community during anaerobic storage and management. Appl. Environ. Microbiol. 72:3578-3585.
39. Reischer, G. H., D. C. Casper, R. Steinborn, R. L. Mach, and A. H. Farn- leitner. 2006. Quantitative PCR method for sensitive detection of ruminant fecal pollution in freshwater and evaluation of this method in Alpine karstic regions. Appl. Environ. Microbiol. 72:5610-5614.
40. Reischer, G. H., D. C. Casper, R. Steinborn, A. H. Farnleitner, and R. L. Mach. 2007. A quantitative real-time PCR assay for the highly sensitive detection of human faecal influence in spring water from a large alpine catchment area. Lett. Appl. Microbiol. 44:351-356.
41. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
42. Savichtcheva, O., N. Okayama, and S. Okabe. 2007. Relationships between Bacteroides 16S rRNA genetic markers and presence of bacterial enteric pathogens and conventional fecal indicators. Water Res. 41:3615-3628.
43. Schloss, P. D., and J. Handelsman. 2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71:1501-1506.
44. Scott, T. M., J. B. Rose, T. M. Jenkins, S. R. Farrah, and J. Lukasik. 2002.
45. Microbial source tracking: current methodology and future directions. Appl. Environ. Microbiol. 68:5796-5803.
46. Seurinck, S., T. Defoirdt, W. Verstraete, and S. D. Siciliano. 2005. Detection and quantification of the human-specific HF183 Bacteroides 16S rRNA genetic marker with real-time PCR for assessment of human faecal pollution in freshwater. Environ. Microbiol. 7:249-259.
47. Simpson, J. M., J. W. Santo Domingo, and D. J. Reasoner. 2002. Microbial source tracking: state of the science. Environ. Sci. Technol. 36:5279-5288.
48. Snell-Castro, R., J. J. Godon, J. P. Delgenes, and P. Dabert. 2005. Characterisation of the microbial diversity in a pig manure storage pit using small subunit rDNA sequence analysis. FEMS Microbiol. Ecol. 52:229-242.
49. Statistical Reference Centre, Canada. 2001. Pigs, provinces. Statistical Reference Centre, Canada, Ottawa, Ontario. http://www40.statcan.gc. ca/L01/cst01/prim51a-eng.htm.
50. Steven, C. E. 1988. Comparative physiology of the vertebrate digestive system. Cambridge University Press, New York, NY.
51. Suzuki, M. T., L. T. Taylor, and E. F. DeLong. 2000. Quantitative analysis of small-subunit rRNA genes in mixed microbial population via 5'-nuclease assays. Appl. Environ. Microbiol. 66:4605-4614.
52. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL-X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
53. Tiquia, S. M. 2005. Microbiological parameters as indicators of compost maturity. J. Appl. Microbiol. 99:816-828.
54. Ufnar, J. A., D. F. Ufnar, S. Y. Wang, and R. D. Ellender. 2007. Development of a swine-specific fecal pollution marker based on host differences in methanogen mcrA genes. Appl. Environ. Microbiol. 73:5209-5217.
55. U.S. Environmental Protection Agency. 2005. Microbial source tracking guide document. EPA Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC.
56. Wheather, D. W. F., D. D. Mara, and J. Oragui. 1979. Indicator systems to distinguish sewage from stormwater runoff and human from animal faecal material, p. 21-27. In A. James and L. Evison (ed.), Biological indicators of water quality. J. Wiley and Sons, Hoboken, NJ.