Quantitative CrAssphage PCR Assays for Human Fecal Pollution Measurement

Environmental Science and Technology

Volumn 51, Issue 16, 2017, Pages 9146-9154

  Stachler, Elyse ^a   Kelty, Catherine ^c   Sivaganesan, Mano ^c   Li, Xiang ^c   Bibby, Kyle ^a,b   Shanks, Orin C ^c  

^a University of Pittsburgh   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; COLIFORM BACTERIA; DATA MINING; POLLUTION; POLYMERASE CHAIN REACTION; QUALITY MANAGEMENT; SCREENING; SEWAGE; WATER CONSERVATION; WATER MANAGEMENT; WATER QUALITY; WATER RESOURCES;

ENVIRONMENTAL WATER; FECAL INDICATOR BACTERIA; FECAL POLLUTION; GENETIC MARKERS; HIGH SPECIFICITY; HUMAN FECAL POLLUTION; POLLUTION SOURCES; RESEARCH TOOLS;

WATER POLLUTION;

DNA; WATER; SEWAGE;

BACTERIUM; BIOASSAY; BIOINFORMATICS; DATA MINING; FECES; GENETIC ANALYSIS; GENETIC MARKER; POLLUTANT SOURCE; POLLUTION MONITORING; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; WATER POLLUTION; WATER QUALITY;

ARTICLE; ASSAY; BACTERIAL GENOME; BACTERIOPHAGE; BIOINFORMATICS; CONTROLLED STUDY; DNA SEQUENCE; FECES; FECES ANALYSIS; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HUMAN; NONHUMAN; POLLUTION MONITORING; POLYMERASE CHAIN REACTION; WATER POLLUTION; WATER QUALITY; WATER SAMPLING; ANIMAL; BACTERIUM; REAL TIME POLYMERASE CHAIN REACTION; SEWAGE;

ANIMALIA; BACTERIA (MICROORGANISMS);

ANIMALS; BACTERIA; FECES; HUMANS; POLYMERASE CHAIN REACTION; REAL-TIME POLYMERASE CHAIN REACTION; SEWAGE; WATER POLLUTION; WATER QUALITY;

EID: 85027470849     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.7b02703     Document Type: Article

References (45)

1. Soller, J. A.; Schoen, M. E.; Bartrand, T.; Ravenscroft, J. E.; Ashbolt, N. J. Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination Water Res. 2010, 44 (16) 4674-4691 10.1016/j.watres.2010.06.049
2. Soller, J. A.; Schoen, M. E.; Varghese, A.; Ichida, A. M.; Boehm, A. B.; Eftim, S.; Ashbolt, N. J.; Ravenscroft, J. E. Human health risk implications of multiple sources of faecal indicator bacteria in a recreational waterbody Water Res. 2014, 66, 254-264 10.1016/j.watres.2014.08.026
3. Boehm, A.; Soller, J., Risks associated with recreational waters: pathogens and fecal indicators. Encyclopedia of Sustainability Science and Technology; Springer Publishing: New York, 2011.
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 Res. 2013, 47 (18) 6812-6828 10.1016/j.watres.2012.12.046
5. Green, H. C.; Haugland, R. A.; Varma, M.; Millen, H. T.; Borchardt, M. A.; Field, K. G.; Walters, W. A.; Knight, R.; Sivaganesan, M.; Kelty, C. A. et al. Improved HF183 quantitative real-time PCR assay for characterization of human fecal pollution in ambient surface water samples Appl. Environ. Microbiol. 2014, 80 (10) 3086-3094 10.1128/AEM.04137-13
6. 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 Environ. Sci. Technol. 2010, 44 (16) 6281-6288 10.1021/es100311n
7. Rodriguez-Lazaro, D.; Cook, N.; Ruggeri, F. M.; Sellwood, J.; Nasser, A.; Nascimento, M. S. J.; D'Agostino, M.; Santos, R.; Saiz, J. C.; Rzeżutka, A. et al. Virus hazards from food, water and other contaminated environments FEMS Microbiol. Rev. 2012, 36 (4) 786-814 10.1111/j.1574-6976.2011.00306
8. Okoh, A. I.; Sibanda, T.; Gusha, S. S. Inadequately treated wastewater as a source of human enteric viruses in the environment Int. J. Environ. Res. Public Health 2010, 7 (6) 2620-2637 10.3390/ijerph7062620
9. Symonds, E. M.; Breitbart, M. Affordable Enteric Virus Detection Techniques Are Needed to Support Changing Paradigms in Water Quality Management Clean: Soil, Air, Water 2015, 43 (1) 8-12 10.1002/clen.201400235
10. Sinclair, R.; Jones, E.; Gerba, C. P. Viruses in recreational water-borne disease outbreaks: A review J. Appl. Microbiol. 2009, 107 (6) 1769-1780 10.1111/j.1365-2672.2009.04367.x
11. Soller, J. A.; Bartrand, T.; Ashbolt, N. J.; Ravenscroft, J.; Wade, T. J. Estimating the primary etiologic agents in recreational freshwaters impacted by human sources of faecal contamination Water Res. 2010, 44 (16) 4736-4747 10.1016/j.watres.2010.07.064
12. Osuolale, O.; Okoh, A. Human enteric bacteria and viruses in five wastewater treatment plants in the Eastern Cape, South Africa J. Infect. Public Health 2017, 10.1016/j.jiph.2016.11.012
13. Zhou, J.; Wang, X. C.; Ji, Z.; Xu, L.; Yu, Z. Source identification of bacterial and viral pathogens and their survival/fading in the process of wastewater treatment, reclamation, and environmental reuse World J. Microbiol. Biotechnol. 2015, 31 (1) 109-120 10.1007/s11274-014-1770-5
14. Qiu, Y.; Lee, B. E.; Neumann, N.; Ashbolt, N.; Craik, S.; Maal-Bared, R.; Pang, X. Assessment of human virus removal during municipal wastewater treatment in Edmonton, Canada J. Appl. Microbiol. 2015, 119 (6) 1729-1739 10.1111/jam.12971
15. Blatchley, E. R.; Gong, W.-L.; Alleman, J. E.; Rose, J. B.; Huffman, D. E.; Otaki, M.; Lisle, J. T. Effects of wastewater disinfection on waterborne bacteria and viruses Water Environ. Res. 2007, 79 (1) 81-92 10.2175/106143006X102024
16. Donaldson, K.; Griffin, D. W.; Paul, J. Detection, quantitation and identification of enteroviruses from surface waters and sponge tissue from the Florida Keys using real-time RT-PCR Water Res. 2002, 36 (10) 2505-2514 10.1016/S0043-1354(01)00479-1
17. Gregory, J. B.; Litaker, R. W.; Noble, R. T. Rapid one-step quantitative reverse transcriptase PCR assay with competitive internal positive control for detection of enteroviruses in environmental samples Appl. Environ. Microbiol. 2006, 72 (6) 3960-3967 10.1128/AEM.02291-05
18. De Leon, R.; Shieh, C.; Baric, R.; Sobsey, M. Detection of enteroviruses and hepatitis A virus in environmental samples by gene probes and polymerase chain reaction. In Proceedings of the 1990 Water Quality Technology Conference; American Water Works Association: Denver, CO, 1990; pp 11-15.
19. Fuhrman, J. A.; Liang, X.; Noble, R. T. Rapid detection of enteroviruses in small volumes of natural waters by real-time quantitative reverse transcriptase PCR Appl. Environ. Microbiol. 2005, 71 (8) 4523-4530 10.1128/AEM.71.8.4523-4530.2005
20. Monpoeho, S.; Maul, A.; Mignotte-Cadiergues, B.; Schwartzbrod, L.; Billaudel, S.; Ferre, V. Best viral elution method available for quantification of enteroviruses in sludge by both cell culture and reverse transcription-PCR Appl. Environ. Microbiol. 2001, 67 (6) 2484-2488 10.1128/AEM.67.6.2484-2488.2001
21. Jothikumar, N.; Cromeans, T. L.; Hill, V. R.; Lu, X.; Sobsey, M. D.; Erdman, D. D. Quantitative real-time PCR assays for detection of human adenoviruses and identification of serotypes 40 and 41 Appl. Environ. Microbiol. 2005, 71 (6) 3131-3136 10.1128/AEM.71.6.3131-3136.2005
22. Heim, A.; Ebnet, C.; Harste, G.; Pring-Åkerblom, P. Rapid and quantitative detection of human adenovirus DNA by real-time PCR J. Med. Virol. 2003, 70 (2) 228-239 10.1002/jmv.10382
23. Jothikumar, N.; Lowther, J. A.; Henshilwood, K.; Lees, D. N.; Hill, V. R.; Vinjé, J. Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples Appl. Environ. Microbiol. 2005, 71 (4) 1870-1875 10.1128/AEM.71.4.1870-1875.2005
24. Kageyama, T.; Kojima, S.; Shinohara, M.; Uchida, K.; Fukushi, S.; Hoshino, F. B.; Takeda, N.; Katayama, K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR J. Clin. Microbiol. 2003, 41 (4) 1548-1557 10.1128/JCM.41.4.1548-1557.2003
25. McQuaig, S. M.; Scott, T. M.; Lukasik, J. O.; Paul, J. H.; Harwood, V. J. Quantification of human polyomaviruses JC virus and BK virus by TaqMan quantitative PCR and comparison to other water quality indicators in water and fecal samples Appl. Environ. Microbiol. 2009, 75 (11) 3379-3388 10.1128/AEM.02302-08
26. IOS. 10705-2: Water Quality. Detection and Enumeration of Bacteriophages-Part 2: Enumeration of Somatic. Coliphages; International Organization for Standardization: Geneva, Switzerland, 2000.
27. EPA. Method 1602: Male-specific (F+) and Somatic Coliphage in Water by Single Agar Layer (SAL) Procedure; EPA: Washington, DC, 2001.
28. Ebdon, J.; Muniesa, M.; Taylor, H. The application of a recently isolated strain of Bacteroides (GB-124) to identify human sources of faecal pollution in a temperate river catchment Water Res. 2007, 41 (16) 3683-3690 10.1016/j.watres.2006.12.020
29. Ebdon, J. E.; Sellwood, J.; Shore, J.; Taylor, H. D. Phages of Bacteroides (GB-124): a novel tool for viral waterborne disease control? Environ. Sci. Technol. 2012, 46 (2) 1163-1169
30. Vijayavel, K.; Fujioka, R.; Ebdon, J.; Taylor, H. Isolation and characterization of Bacteroides host strain HB-73 used to detect sewage specific phages in Hawaii Water Res. 2010, 44 (12) 3714-3724 10.1016/j.watres.2010.04.012
31. Rosario, K.; Symonds, E. M.; Sinigalliano, C.; Stewart, J.; Breitbart, M. Pepper mild mottle virus as an indicator of fecal pollution Appl. Environ. Microbiol. 2009, 75 (22) 7261-7267 10.1128/AEM.00410-09
32. 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. et al. Performance of viruses and bacteriophages for fecal source determination in a multi-laboratory, comparative study Water Res. 2013, 47 (18) 6929-6943 10.1016/j.watres.2013.04.064
33. Staley, C.; Gordon, K. V.; Schoen, M. E.; Harwood, V. J. Performance of two quantitative PCR methods for microbial source tracking of human sewage and implications for microbial risk assessment in recreational waters Appl. Environ. Microbiol. 2012, 78 (20) 7317-7326 10.1128/AEM.01430-12
34. Dutilh, B. E.; Cassman, N.; McNair, K.; Sanchez, S. E.; Silva, G. G.; Boling, L.; Barr, J. J.; Speth, D. R.; Seguritan, V.; Aziz, R. K. et al. A highly abundant bacteriophage discovered in the unknown sequences of human faecal metagenomes Nat. Commun. 2014, 5, 1-11 10.1038/ncomms5498
35. Stachler, E.; Bibby, K. Metagenomic Evaluation of the Highly Abundant Human Gut Bacteriophage CrAssphage for Source Tracking of Human Fecal Pollution Environ. Sci. Technol. Lett. 2014, 1 (10) 405-409 10.1021/ez500266s
36. Minot, S.; Bryson, A.; Chehoud, C.; Wu, G. D.; Lewis, J. D.; Bushman, F. D. Rapid evolution of the human gut virome Proc. Natl. Acad. Sci. U. S. A. 2013, 110 (30) 12450-12455 10.1073/pnas.1300833110
37. Mizuno, C. M.; Ghai, R.; Rodriguez-Valera, F. Evidence for metaviromic islands in marine phages Front. Microbiol. 2014, 5, 1-10 10.3389/fmicb.2014.00027
38. Ye, J.; Coulouris, G.; Zaretskaya, I.; Cutcutache, I.; Rozen, S.; Madden, T. L. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction BMC Bioinf. 2012, 13 (1) 134 10.1186/1471-2105-13-134
39. Shanks, O. C.; Kelty, C. A.; Sivaganesan, M.; Varma, M.; Haugland, R. A. Quantitative PCR for genetic markers of human fecal pollution Appl. Environ. Microbiol. 2009, 75 (17) 5507-5513 10.1128/AEM.00305-09
40. 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 Syst. Appl. Microbiol. 2010, 33 (6) 348-357 10.1016/j.syapm.2010.06.001
41. Sivaganesan, M.; Haugland, R. A.; Chern, E. C.; Shanks, O. C. Improved strategies and optimization of calibration models for real-time PCR absolute quantification Water Res. 2010, 44 (16) 4726-4735 10.1016/j.watres.2010.07.066
42. Shanks, O. C.; Kelty, C. A.; Oshiro, R.; Haugland, R. A.; Madi, T.; Brooks, L.; Field, K. G.; Sivaganesan, M. Data acceptance criteria for standardized human-associated fecal source identification quantitative real-time PCR methods Appl. Environ. Microbiol. 2016, 82 (9) 2773-2782 10.1128/AEM.03661-15
43. Liang, Y.; Zhang, W.; Tong, Y.; Chen, S. CrAssphage is not associated with diarrhoea and has high genetic diversity Epidemiol. Infect. 2016, 144 (16) 3549-3553 10.1017/S095026881600176X
44. Reyes, A.; Semenkovich, N. P.; Whiteson, K.; Rohwer, F.; Gordon, J. I. Going viral: next-generation sequencing applied to phage populations in the human gut Nat. Rev. Microbiol. 2012, 10 (9) 607-617 10.1038/nrmicro2853
45. Minot, S.; Wu, G. D.; Lewis, J. D.; Bushman, F. D. Conservation of gene cassettes among diverse viruses of the human gut PLoS One 2012, 7 (8) e42342 10.1371/journal.pone.0042342