Lachnospiraceae and bacteroidales alternative fecal indicators reveal chronic human sewage contamination in an Urban harbor

Applied and Environmental Microbiology

Volumn 77, Issue 19, 2011, Pages 6972-6981

  Newton, Ryan J ^a   VandeWalle, Jessica L ^a   Borchardt, Mark A ^b   Gorelick, Marc H ^c,d   McLellan, Sandra L ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d CHILDREN S HOSPITAL OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; COMBINED SEWER OVERFLOWS; FECAL INDICATOR BACTERIA; FECAL INDICATORS; FECAL POLLUTION; GENETIC MARKERS; HEAVY RAIN EVENT; HUMAN ADENOVIRUS; HUMAN FECAL; HUMAN FECAL POLLUTION; HUMAN HEALTH RISKS; HUMAN PATHOGENS; MICROBIAL COMMUNITIES; MICROBIAL COMMUNITY COMPOSITION; PHYLOTYPES; QUANTITATIVE PCR; SEQUENCE ANALYSIS; SEWAGE CONTAMINATION; URBAN WATERS;

ASSAYS; COMBINED SEWERS; CONTAMINATION; ESCHERICHIA COLI; GENES; HEALTH RISKS; MICROORGANISMS; POLLUTION; POLYMERASE CHAIN REACTION; RNA; WATER ANALYSIS;

SEWAGE;

BACTERIAL DNA; PRIMER DNA; RIBOSOME DNA; RNA 16S;

BACTERIUM; COMMUNITY COMPOSITION; DATABASE; FECES; GENETIC ANALYSIS; GENETIC MARKER; HARBOR; HEALTH RISK; MICROBIAL COMMUNITY; POLYMERASE CHAIN REACTION; PROBABILITY; PUBLIC HEALTH; SEWAGE; URBAN AREA;

ANIMAL; ARTICLE; BACTEROIDETES; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; EVALUATION; GENETICS; GRAM POSITIVE BACTERIUM; HUMAN; ISOLATION AND PURIFICATION; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; SEWAGE;

ANIMALS; BACTERIOLOGICAL TECHNIQUES; BACTEROIDETES; DNA PRIMERS; DNA, BACTERIAL; DNA, RIBOSOMAL; ENVIRONMENTAL MICROBIOLOGY; GRAM-POSITIVE BACTERIA; HUMANS; MOLECULAR SEQUENCE DATA; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEWAGE;

EID: 82955227659     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.05480-11     Document Type: Article

References (60)

1. Ahn, J. H., et al. 2005. Coastal water quality impact of stormwater runoff from an urban watershed in Southern California. Environ. Sci. Technol. 39:5940-5953.
2. Andersson, A. F., L. Riemann, and S. Bertilsson. 2010. Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. ISME J. 4:171-181.
3. Arnone, R. D., and J. P. Walling. 2007. Waterborne pathogens in urban watersheds. J. Water Health 5:149-162.
4. 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.
5. Barnes, B., and D. M. Gordon. 2004. Coliform dynamics and the implications for source tracking. Environ. Microbiol. 6:501-509.
6. Bergholz, P. W., J. D. Noar, and D. H. Buckley. 2011. Environmental patterns are imposed on the population structure of Escherichia coli after fecal deposition. Appl. Environ. Microbiol. 77:211-219.
7. Bernhard, A. E., and K. G. Field. 2000. A PCR assay to discriminate human and ruminant feces on the basis of host differences in Bacteroides-Prevotella genes encoding 16S rRNA. Appl. Environ. Microbiol. 66:4571-4574.
8. Beversdorf, L. J., S. M. Bornstein-Forst, and S. L. McLellan. 2007. The potential for beach sand to serve as a reservoir for Escherichia coli and the physical influences on cell die-off. J. Appl. Microbiol. 102:1372-1381.
9. Cole, J. R., et al. 2003. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 31:442-443.
10. Cromeans, T., et al. 2005. Development of molecular methods to detect infectious viruses in water. Report no. 90995F. American Water Works Association Research Foundation (AwwaRF), Denver, CO.
11. Dethlefsen, L., S. Huse, M. L. Sogin, and D. A. Relman. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6:2383-2400.
12. Dick, L. K., et al. 2005. Host distributions of uncultivated fecal Bacteroidales bacteria reveal genetic markers for fecal source identification. Appl. Environ. Microbiol. 71:3184-3191.
13. Dick, L. K., and K. G. Field. 2004. Rapid estimation of numbers of fecal Bacteroidetes by use of a quantitative PCR assay for 16S rRNA genes. Appl. Environ. Microbiol. 70:5695-5697.
14. Dufour, A. P. 1984. Bacterial indicators of recreational water quality. Can. J. Public Health 75:49-56.
15. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175-185.
16. Field, K. G., and M. Samadpour. 2007. Fecal source tracking, the indicator paradigm, and managing water quality. Water Res. 41:3517-3538.
17. Gaffield, S. J., R. L. Goo, L. A. Richards, and R. J. Jackson. 2003. Public health effects of inadequately managed stormwater runoff. Am. J. Public Health 93:1527-1533.
18. Gordon, D. M. 2001. Geographical structure and host specificity in bacteria and the implications for tracing the source of coliform contamination. Microbiology 147:1079-1085.
19. Hamilton, M. J., T. Yan, and M. J. Sadowsky. 2006. Development of gooseand duck-specific DNA markers to determine sources of Escherichia coli in waterways. Appl. Environ. Microbiol. 72:4012-4019.
20. Ishii, S., D. L. Hansen, R. E. Hicks, and M. J. Sadowsky. 2007. Beach sand and sediments are temporal sinks and sources of Escherichia coli in Lake Superior. Environ. Sci. Technol. 41:2203-2209.
21. Kildare, B. J., et al. 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.
22. Kuo, D. W., F. Simmons, and I. Xagoraraki. 2009. A new set of PCR assays for the identification of multiple human adenovirus species in environmental samples. J. Appl. Microbiol. 107:1219-1229.
23. Lambertini, E., et al. 2008. Concentration of enteroviruses, adenoviruses, and noroviruses from drinking water by use of glass wool filters. Appl. Environ. Microbiol. 74:2990-2996.
24. Layton, A., et al. 2006. Development of Bacteroides 16S rRNA gene Taq-Man-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water. Appl. Environ. Microbiol. 72:4214-4224.
25. Lu, J. R., J. W. Santo Domingo, R. Lamendella, T. Edge, and S. Hill. 2008. Phylogenetic diversity and molecular detection of bacteria in gull feces. Appl. Environ. Microbiol. 74:3969-3976.
26. Ludwig, W., and K. H. Schleifer. 2000. How quantitative is quantitative PCR with respect to cell counts? Syst. Appl. Microbiol. 23:556-562.
27. Ludwig, W., et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
28. Matsuki, T., et al. 2002. Development of 16S rRNA-gene-targeted groupspecific primers for the detection and identification of predominant bacteria in human feces. Appl. Environ. Microbiol. 68:5445-5451.
29. McLellan, S. L., S. M. Huse, S. R. Mueller-Spitz, E. N. Andreishcheva, and M. L. Sogin. 2010. Diversity and population structure of sewage-derived microorganisms in wastewater treatment plant influent. Environ. Microbiol. 12:378-392.
30. Mueller-Spitz, S. R., G. W. Goetz, and S. L. McLellan. 2009. Temporal and spatial variability in nearshore bacterioplankton communities of Lake Michigan. FEMS Microbiol. Ecol. 67:511-522.
31. Noble, R. T., et al. 2003. Use of viral pathogens and indicators to differentiate between human and non-human fecal contamination in a microbial source tracking comparison study. J. Water Health 1:195-207.
32. Okabe, S., and Y. Shimazu. 2007. Persistence of host-specific Bacteroides-Prevotella 16S rRNA genetic markers in environmental waters: effects of temperature and salinity. Appl. Microbiol. Biotechnol. 76:935-944.
33. Parker, J. K., D. McIntyre, and R. T. Noble. 2010. Characterizing fecal contamination in stormwater runoff in coastal North Carolina, U. S. A. Water Res. 44:4186-4194.
34. Peterson, J., et al. 2009. The NIH human microbiome project. Genome Res. 19:2317-2323.
35. Pina, S., M. Puig, F. Lucena, J. Jofre, and R. Girones. 1998. Viral pollution in the environment and in shellfish: human adenovirus detection by PCR as an index of human viruses. Appl. Environ. Microbiol. 64:3376-3382.
36. Pruesse, E., et al. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35:7188-7196.
37. Pruss, A. 1998. Review of epidemiological studies on health effects from exposure to recreational water. Int. J. Epidemiol. 27:1-9.
38. Qin, J. J., et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59-65.
39. Roesch, L. F., et al. 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1:283-290.
40. Rutsch, M., et al. 2008. Towards a better understanding of sewer exfiltration. Water Res. 42:2385-2394.
41. Sauer, E. P., P. A. Bower, M. J. Bootsma, and S. L. McLellan. 2011. Detection of the human specific Bacteroides genetic marker provides evidence of widespread sewage contamination of stormwater in the urban environment. Water Res. 45:4081-4091.
42. Schoen, M. E., and N. J. Ashbolt. 2010. Assessing pathogen risk to swimmers at non-sewage impacted recreational beaches. Environ. Sci. Technol. 44: 2286-2291.
43. Sedmak, G., D. Bina, and J. MacDonald. 2003. Assessment of an enterovirus sewage surveillance system by comparison of clinical isolates with sewage isolates from Milwaukee, Wisconsin, collected August 1994 to December 2002. Appl. Environ. Microbiol. 69:7181-7187.
44. Sedmak, G., D. Bina, J. MacDonald, and L. Couillard. 2005. Nine-year study of the occurrence of culturable viruses in source water for two drinking water treatment plants and the influent and effluent of a wastewater treatment plant in Milwaukee, Wisconsin (August 1994 through July 2003). Appl. Environ. Microbiol. 71:1042-1050.
45. Sercu, B., L. C. Van De Werfhorst, J. Murray, and P. A. Holden. 2009. Storm drains are sources of human fecal pollution during dry weather in three urban Southern California watersheds. Environ. Sci. Technol. 43:293-298.
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. Shanks, O. C., et al. 2011. Community structure of cattle fecal bacteria from different animal feeding operations. Appl. Environ. Microbiol. 77:2992-3001.
48. Shanks, O. C., C. A. Kelty, M. Sivaganesan, M. Varma, and R. A. Haugland. 2009. Quantitative PCR for genetic markers of human fecal pollution. Appl. Environ. Microbiol. 75:5507-5513.
49. Shanks, O. C., et al. 2006. Basin-wide analysis of the dynamics of fecal contamination and fecal source identification in Tillamook Bay, Oregon. Appl. Environ. Microbiol. 72:5537-5546.
50. Shanks, O. C., et al. 2010. Performance of PCR-based assays targeting Bacteroidales genetic markers of human fecal pollution in sewage and fecal samples. Environ. Sci. Technol. 44:6281-6288.
51. Stoeckel, D. M., and V. J. Harwood. 2007. Performance, design, and analysis in microbial source tracking studies. Appl. Environ. Microbiol. 73:2405-2415.
52. Turnbaugh, P. J., et al. 2009. A core gut microbiome in obese and lean twins. Nature 457:480-485.
53. Turnbaugh, P. J., et al. 2007. The human microbiome project. Nature 449: 804-810.
54. U.S. Environmental Protection Agency. 2002. Method 1600: enterococci in water by membrane filtration using membrane-Enterococcus indoxyl--Dgucoside agar (mEI). U.S. Environmental Protection Agency, Office of Water, Washington, DC.
55. U.S. Environmental Protection Agency. 2002. Method 1603: Escherichia coli (E. coli) in water by membrane filtration using modified membrane-thermotolerant Escherichia coli agar (modified mTEC). U.S. Environmental Protection Agency, Office of Water, Washington, DC.
56. U.S. Environmental Protection Agency. 2009. National Water Quality Inventory: Report to Congress, 2004 Reporting Cycle. U.S. Environmental Protection Agency, Office of Water, Washington, DC.
57. U.S. Environmental Protection Agency. 2004. Report to Congress: Impacts and Control of CSOs and SSOs. U.S. Environmental Protection Agency, Office of Water, Washington, DC.
58. Walters, S. P., V. P. J. Gannon, and K. G. Field. 2007. Detection of Bacteroidales fecal indicators and the zoonotic pathogens E. coli O157:H7, Salmonella, and Campylobacter in river water. Environ. Sci. Technol. 41:1856-1862.
59. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267.
60. Whitman, R. L., D. A. Shively, H. Pawlik, M. B. Nevers, and M. N. Byappanahalli. 2003. Occurrence of Escherichia coli and enterococci in Cladophora (Chlorophyta) in nearshore water and beach sand of Lake Michigan. Appl. Environ. Microbiol. 69:4714-4719.