Performance of human fecal anaerobe-associated PCR-based assays in a multi-laboratory method evaluation study

Water Research

Volumn 47, Issue 18, 2013, Pages 6897-6908

  Layton, Blythe A ^a   Cao, Yiping ^a   Ebentier, Darcy L ^b   Hanley, Kaitlyn ^b   Ballesté, Elisenda ^c   Brandão, João ^d   Byappanahalli, Muruleedhara ^e   Converse, Reagan ^f,g   Farnleitner, Andreas H ^h   Gentry Shields, Jennifer ⁱ   Gidley, Maribeth L ^j   Gourmelon, Michèle ^k   Lee, Chang Soo ^l   Lee, Jiyoung ^l   Lozach, Solen ^k   Madi, Tania ^m   Meijer, Wim G ^c   Noble, Rachel ^f   Peed, Lindsay ⁿ   Reischer, Georg H ^h   Rodrigues, Raquel ^d   Rose, Joan B ^o   Schriewer, Alexander ^p   Sinigalliano, Chris ^q   Srinivasan, Sangeetha ^o   Stewart, Jill ⁱ   Van De Werfhorst, Laurie C ^r   Wang, Dan ^s   Whitman, Richard ^e   Wuertz, Stefan ^p,t   Jay, Jenny ^b   Holden, Patricia A ^r   Boehm, Alexandria B ^s   Shanks, Orin ⁿ   Griffith, John F ^a   more..

^a SOUTHERN CALIFORNIA COASTAL WATER RESEARCH PROJECT   (United States)

^b Department of Civil and Environmental Engineering   (United States)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

^e U S GEOLOGICAL SURVEY   (United States)

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

^g OAK RIDGE INSTITUTE FOR SCIENCE AND EDUCATION   (United States)

^h VIENNA UNIVERSITY OF TECHNOLOGY   (Austria)

ⁱ UNIVERSITY OF NORTH CAROLINA   (United States)

^j UNIVERSITY OF MIAMI   (United States)

^k IFREMER   (France)

^l OHIO STATE UNIVERSITY   (United States)

^m Source Molecular Corporation   (United States)

ⁿ U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^o MICHIGAN STATE UNIVERSITY   (United States)

^p Davis   (United States)

^q ATLANTIC OCEANOGRAPHIC AND METEOROLOGICAL LABORATORY   (United States)

^r UNIVERSITY OF CALIFORNIA   (United States)

^s Nanyang Technological University ^*  (United States)

^t NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

more..

Author keywords

Bacteroidales; Bacteroides; Microbial source tracking; QPCR; Water quality

Indexed keywords

POLYMERASE CHAIN REACTION; SEWAGE; WATER QUALITY;

BACTEROIDALES; BACTEROIDES; BACTEROIDES THETAIOTAOMICRON; FECAL CONCENTRATIONS; HUMAN FECAL MATERIALS; LABORATORY PROTOCOLS; MICROBIAL SOURCE TRACKING; QPCR;

LABORATORIES;

BACTERIAL DNA;

ANTHROPOGENIC SOURCE; CONCENTRATION (COMPOSITION); FECES; LABORATORY METHOD; MICROBIOLOGY; PERFORMANCE ASSESSMENT; POLLUTANT SOURCE; POLYMERASE CHAIN REACTION; WASTEWATER; WATER QUALITY;

ANAEROBE; ARTICLE; BACTEROIDES THETAIOTAOMICRON; DNA EXTRACTION; ENTEROCOCCUS; ESCHERICHIA COLI; FECES ANALYSIS; HUMAN; METHANOBREVIBACTER SMITHII; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SENSITIVITY AND SPECIFICITY; SEWAGE; WASTE WATER; WATER QUALITY;

BACTEROIDALES; BACTEROIDES; BACTEROIDES THETAIOTAOMICRON; METHANOBREVIBACTER SMITHII;

BACTEROIDALES; BACTEROIDES; MICROBIAL SOURCE TRACKING; QPCR; WATER QUALITY;

BACTERIA, ANAEROBIC; CALIFORNIA; DNA, BACTERIAL; ENVIRONMENTAL MONITORING; FECES; HUMANS; LIMIT OF DETECTION; REAL-TIME POLYMERASE CHAIN REACTION; WASTE WATER; WATER MICROBIOLOGY; WATER POLLUTION;

EID: 84887163231     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2013.05.060     Document Type: Article

References (39)

1. Ahmed W., Masters N., Toze S. Consistency in the host specificity and host sensitivity of the Bacteroides HF183 marker for sewage pollution tracking. Letters in Applied Microbiology 2012, 55(4):283-289.
2. Bernhard A.E., Field K. A PCR assay to discriminate human and ruminant feces on the basis of host differences in Bacteroides-Prevotella genes encoding 16S rRNA. Applied and Environmental Microbiology 2000, 66(10):4571-4574.
3. Boehm A.B., Soller J.A. Risks associated with recreational waters: pathogens and fecal indicators. Encyclopedia of Sustainability Science and Technology 2011, Springer. R.A. Meyers (Ed.).
4. Boehm A.B., Van De Werfhorst L.C., Griffith J.F., Holden P.A., Jay J.A., Shanks O.C., Wang D., Weisberg S.B. Performance of forty-one microbial source tracking methods: a twenty-seven lab evaluation study. Water Research 2013, 47(18):6812-6828.
5. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 2009, 55(4):611-622.
6. Cao Y., Van De Werfhorst L.C., Dubinsky E.A., Badgley B.D., Sadowsky M.J., Andersen G.L., Griffith J.F., Holden P.A. Evaluation of molecular community analysis methods fordiscerning fecal sources and human waste. Water Research 2013, 47(18):6849-6861.
7. Chern E.C., Siefring S., Paar J., Doolittle M., Haugland R.A. Comparison of quantitative PCR assays for Escherichia coli targeting ribosomal RNA and single copy genes. Letters in Applied Microbiology 2011, 52(3):298-306.
8. Converse R., Blackwood A.D., Kirsb M., Griffith J.F., Noble R. Rapid QPCR-based assay for fecal Bacteroides spp. as a tool for assessing fecal contamination in recreational waters. Water Research 2009, 43(19):4828-4837.
9. Ebentier D.L., Hanley K.T., Cao Y., Badgley B.D., Boehm A.B., Ervin J.S., Goodwin K.D., Gourmelon M., Griffith J.F., Holden P.A., Kelty C.A., Lozach S., McGee C.D., Peed L.A., Raith M.R., Sadowsky M.J., Scott E., Santo Domingo J., Sinigalliano C., Shanks O.C., Van De Werfhorst L.C., Wang D., Wuertz S., Jay J.A. Evaluation of the repeatability and reproducibility of a suite of qPCR-based microbial source tracking methods. Water Research 2013, 47(18):6839-6848.
10. Ervin J.S., Russell T.L., Layton B.A., Yamahara K.M., Wang D., Sassoubre L.M., Cao Y., Kelty C.A., Sivaganesan M., Boehm A.B., Holden P.A., Weisberg S.B., Shanks O.C. Characterization of fecal concentrations in human and other animal sources by physical, culture, and quantitative real-time PCR methods. Water Research 2013, 47(18):6873-6882.
11. Field K., Samadpour M. Fecal source tracking, the indicator paradigm, and managing water quality. Water Research 2007, 41(16):3517-3538.
12. Gawler A.H., Beecher J.E., Brandão J., Carroll N.M., Falcão L., Gourmelon M., Masterson B., Nunes B., Porter J., Rincé A., Rodrigues R., Thorp M., Walters J.M., Meijer W.G. Validation of host-specific bacteriodales 16S rRNA genes as markers to determine the origin of faecal pollution in Atlantic rim countries of the European Union. Water Research 2007, 41(16):3780-3784.
13. Griffith J.F., Weisberg S., McGee C. Evaluation of microbial source tracking methods using mixed fecal sources in aqueous test samples. Journal of Water and Health 2003, 1(7):141-151.
14. Harwood V.J., Boehm A.B., Sassoubre L.M., Vijayavel K., Stewart J.R., Fong T.-T., Caprais M.P., Converse R.R., Diston D., Ebdon J., Fuhrman J.A., Gourmelon M., Gentry-Shields J., Griffith J.F., Kashian D.R., Noble R.T., Taylor H., Wicki M. Performance of viruses and bacteriophages for fecal source determination in a multi-laboratory, comparative study. Water Research 2013, 47(18):6829-6943.
15. Haugland R., Siefring S., Wymer L., Brenner K., Dufour A. Comparison of Enterococcus measurements in freshwater at two recreational beaches by quantitative polymerase chain reaction and membrane filter culture analysis. Water Research 2005, 39(4):559-568.
16. Haugland R.A., Varma M., Sivaganesan M., Kelty C., Peed L., Shanks O.C. Evaluation of genetic markers from the 16S rRNA gene V2 region for use in quantitative detection of selected Bacteroidales species and human fecal waste by qPCR. Systematic and Applied Microbiology 2010, 33(6):348-357.
17. Johnston C., Ufnar J.A., Griffith J.F., Gooch J.A., Stewart J.R. A real-time qPCR assay for the detection of the nifH gene of Methanobrevibacter smithii, a potential indicator of sewage pollution. Journal of Applied Microbiology 2010, 109(6):1946-1956.
18. Kelty C.A., Varma M., Sivaganesan M., Haugland R.A., Shanks O.C. Distribution of genetic marker concentrations for fecal indicator bacteria in sewage and animal feces. Applied and Environmental Microbiology 2012, 78(12):4225-4232.
19. Kildare B.J., Leutenegger C.M., McSwain B.S., Bambic D.G., Rajal V.B., Wuertz S. 16S rRNA-based assays for quantitative detection of universal, human-, cow-, and dog-specific fecal Bacteroidales: a Bayesian approach. Water Research 2007, 41(16):3701-3715.
20. Layton A., McKay L., Williams D., Garrett V., Gentry R., Sayler G. Development of Bacteroides 16S rRNA gene TaqMan-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water. Applied and Environmental Microbiology 2006, 72(6):4214-4224.
21. Lee C.S., Lee J. Evaluation of new gyrB-based real-time PCR system for the detection of B. fragilis as an indicator of human-specific fecal contamination. Journal of Microbiological Methods 2010, 82(3):311-318.
22. Matsuki T., Watanabe K., Fujimoto J., Miyamoto Y., Takada T., Matsumoto K., Oyaizu H., Tanaka R. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Applied and Environmental Microbiology 2002, 68(11):5445-5451.
23. Mauffret A., Caprais M.P., Gourmelon M. Relevance of Bacteroidales and F-specific RNA bacteriophages for efficient fecal contamination tracking at the level of a catchment in France. Applied and Environmental Microbiology 2012, 78(15):5143-5152.
24. McLellan S.L., Huse S.M., Mueller-Spitz S.R., Andreishcheva E.N., Sogin M.L. Diversity and population structure of sewage-derived microorganisms in wastewater treatment plant influent. Environmental Microbiology 2010, 12(2):378-392.
25. Pan Y., Bodrossy L., Frenzel P., Hestnes A.G., Krause S., Luke C., Meima-Franke M., Siljanen H., Svenning M.M., Bodelier P.L.E. Impacts of inter- and intralaboratory variations on the reproducibility of microbial community analyses. Applied and Environmental Microbiology 2010, 76(22):7451-7458.
26. Raith M.R., Kelty C.A., Griffith J.F., Schriewer A., Wuertz S., Mieszkin S., Gourmelon M., Reischer G.H., Farnleitner A.H., Ervin J., Holden P.A., Jay J.A., Boehm A.B., Rose J.B., Meijer W.G., Sivaganesan M., Shanks O.C. Comparison of PCR and quantitative real-time PCR methods for the characterization of ruminant and cattle fecal pollution sources. Water Research 2013, 47(18):6921-6928.
27. Reischer G., Kasper D., Steinborn R., Farnleitner A., Mach R. A quantitative real-time PCR assay for the highly sensitive and specific detection of human faecal influence in spring water from a large alpine catchment area. Letters in Applied Microbiology 2007, 44(4):351-356.
28. Roslev P., Bukh A.S. State of the art molecular markers for fecal pollution source tracking in water. Applied Microbiology and Biotechnology 2011, 89(5):1341-1355.
29. Sauer E.P., VandeWalle J.L., Bootsma M.J., McLellan S.L. Detection of the human specific Bacteroides genetic marker provides evidence of widespread sewage contamination of stormwater in the urban environment. Water Research 2011, 45(14):4081-4091.
30. Seurinck S., Defoirdt T., Verstraete W., Siciliano S. 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. Environmental Microbiology 2005, 7(2):249-259.
31. Shanks O.C., Kelty C.A., Sivaganesan M., Varma M., Haugland R.A. Quantitative PCR for genetic markers ofhuman fecal pollution. Applied and Environmental Microbiology 2009, 75(17):5507-5513.
32. Shanks O.C., White K., Kelty C.A., Sivaganesan M., Blannon J., Meckes M., Varma M., Haugland R.A. Performance of PCR-based assays targeting Bacteroidales genetic markers of human fecal pollution in sewage and fecal samples. Environmental Science and Technology 2010, 44(16):6281-6288.
33. Siefring S., Varma M., Atikovic E., Wymer L., Haugland R.A. Improved real-time PCR assays for the detection of fecal indicator bacteria in surface waters with different instrument and reagent systems. Journal of Water and Health 2008, 6(2):225-237.
34. Sinigalliano C.D., Ervin J.S., Van De Werfhorst L.C., Badgley B.D., Ballesté E., Bartkowiak J., Boehm A.B., Byappanahalli M.N., Goodwin K.D., Gourmelon M., Griffith J.F., Holden P.A., Jay J.A., Layton B.A., Lee C., Lee J., Meijer W.G., Noble R.T., Raith M.R., Ryu H., Sadowsky M.J., Schriewer A., Wang D., Wanless D., Whitman R.L., Wuertz S., Santo Domingo J.W. Multi-laboratory evaluations of the performance of Catellicoccus marimammalium PCR assays developed to target gull fecal sources. Water Research 2013, 47(18):6883-6896.
35. Srinivasan S., Aslan A., Xagoraraki I., Alocilja E., Rose J.B. Escherichia coli, enterococci, and Bacteroides thetaiotaomicron qPCR signals through wastewater and septage treatment. Water Research 2011, 45(8):2561-2572.
36. Stapleton C.M., Kay D., Wyer M.D., Davies C., Watkins J., Kay C., McDonald A.T., Porter J., Gawler A. Evaluating the operational utility of a Bacteroidales quantitative PCR-based MST approach in determining the source of faecal indicator organisms at a UK bathing water. Water Research 2009, 43(19):4888-4899.
37. Stewart J.R., Boehm A.B., Dubinsky E.A., Fong T.-T., Goodwin K.D., Griffith J.F., Noble R.T., Shanks O.C., Vijayavel K., Weisberg S.B. Recommendations following a multi-laboratory comparison of microbial source tracking methods. Water Research 2013, 47(18):6829-6938.
38. USEPA Microbial Source Tracking Guide Document 2005, (No.EPA/600-R-05-064), U.S. Environmental Protection Agency, Office of Research and Development, National Risk Management Research Laboratory, Cincinnati, OH.
39. Yampara-Iquise H., Zheng G., Jones J.E., Carson C.A. Use of a Bacteroides thetaiotaomicron-specific alpha-1-6, mannanase quantitative PCR to detect human faecal pollution in water. Journal of Applied Microbiology 2008, 105(5):1686-1693.