Dynamics of fecal indicator bacteria, bacterial pathogen genes, and organic wastewater contaminants in the Little Calumet River-Portage Burns Waterway, Indiana

Journal of Great Lakes Research

Volumn 39, Issue 2, 2013, Pages 317-326

  Haack, Sheridan K ^a   Duris, Joseph W ^a  

^a U S GEOLOGICAL SURVEY   (United States)

Author keywords

Emerging contaminants; Escherichia coli; Fecal indicator bacteria; Little Calumet River Portage Burns Waterway; Nearshore; Recreational water quality

Indexed keywords

EMERGING CONTAMINANT; FECAL INDICATOR BACTERIA; LITTLE CALUMET RIVER-PORTAGE BURNS WATERWAY; NEARSHORES; RECREATIONAL WATER QUALITY;

ANIMALS; BEACHES; CHLORINE COMPOUNDS; COASTAL ENGINEERING; ECOLOGY; EFFLUENTS; ESCHERICHIA COLI; GENES; LAKES; ORGANIC CHEMICALS; PATHOGENS; RIVERS; TURBIDITY; WATER ANALYSIS; WATER QUALITY; WATERSHEDS;

RIVER POLLUTION;

ANTHROPOGENIC EFFECT; CORRELATION; FRESHWATER ECOSYSTEM; GENE EXPRESSION; MICROBIAL COMMUNITY; PATHOGEN; RIVER PLUME; WATER QUALITY;

GREAT LAKES [NORTH AMERICA]; INDIANA; LAKE MICHIGAN; UNITED STATES;

ANIMALIA; BACTERIA (MICROORGANISMS); ENTEROCOCCUS; ESCHERICHIA COLI;

EID: 84878113927     PISSN: 03801330     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jglr.2013.03.015     Document Type: Article

References (70)

1. Aslan A., Xagoraraki I., Simmons F.J., Rose J.B., Dorevitch S. Occurrence of adenovirus and other enteric viruses in limited-contact freshwater recreational areas and bathing waters. J. Appl. Microbiol. 2011, 111:1250-1261.
2. Bauer L.M., Alm E.W. Escherichia coli toxin and attachment genes in sand at Great Lakes recreational beaches. J. Great Lakes Res. 2012, 38:129-133.
3. Benham B.L., Baffaut C., Zeckoski R.W., Mankin K.R., Pachepsky Y.A., Sadeghi A.M., Brannan K.M., Soupir M.L., Habersack M.J. Modeling bacteria fate and transport in watersheds to support TMDLs. Trans. ASABE 2006, 49:987-1002.
4. Beutin L., Kruger U., Krause G., Miko A., Martin A., Strauch E. Evaluation of major types of Shiga toxin 2e-producing Escherichia coli bacteria present in food, pigs, and the environment as potential pathogens for humans. Appl. Environ. Microbiol. 2008, 74:4806-4816.
5. Boehm A.B., Ashbolt N.J., Colford J.M., Dunbar L.E., Fleming L.E., Gold M.A., Hansel J.A., Hunter P.R., Ichida A.M., McGee C.D., Soller J.A., Weisberg S.B. A sea change ahead for recreational water quality criteria. J. Water Health 2009, 7:9-20.
6. c is the most common Shiga toxin 1 subtype among Shiga toxin-producing Escherichia coli isolates from sheep but not among isolates from cattle. J. Clin. Microbiol. 2003, 41:926-936.
7. Byappanahalli M.N., Fowler M., Shively D.A., Whitman R.L. Ubiquity and persistence of Escherichia coli in a Midwestern coastal stream. Appl. Environ. Microbiol. 2003, 69:4549-4555.
8. Byappanahalli M.N., Whitman R.L., Shively D.A., Sadowsky M.J., Ishii S. Population structure, persistence, and seasonality of autochthonus Escherichia coli in temperate, coastal forest soil from a Great Lakes watershed. Environ. Microbiol. 2006, 8:504-513.
9. Earth Tech Inc. Little Calumet and Portage Burns Waterway TMDL for E. coli bacteria accessed at, (on Sept. 28, 2012). http://www.in.gov/idem/water/planbr/wqs/tmdl/documents.htm.
10. Environmental Systems Research Institute (ESRI) Tele Atlas North America, Inc 2006, U.S. Census Block Groups, ESRI Data & Maps Series, Redlands, California.
11. Etoh Y., Murakami K., Ichihara S., Sera N., Hamasaki M., Takenaka S., Horikawa K., Kawano K., Takeishi T., Kuwana Y., Inoue A., Nagatsu Y., Hira Y., Takahashi M., Ito K. Isolation of Shiga toxin 2f-producing Escherichia coli (O115:HNM) from an adult symptomatic patient in Fukuoka Prefecture Japan. Jpn. J. Infect. Dis. 2009, 62:315-317.
12. Field K.G., Samadpour M. Fecal source tracking, the indicator paradigm, and managing water quality. Water Res. 2007, 41:3517-3538.
13. Francy D.S. Use of predictive models and rapid methods to nowcast bacteria levels at coastal beaches. Aquat. Ecosyst. Health Manag. 2009, 12:177-182.
14. Fremaux B., Gritzfeld J., Boa T., Yost C.K. Evaluation of host-specific Bacteroidales 16S rRNA gene markers as a complementary tool for detecting fecal pollution in a prairie watershed. Water Res. 2009, 43:4838-4849.
15. Ge Z., Frick W.E. Time-frequency analysis of beach bacteria variations and its implication for recreational water quality modeling. Environ. Sci. Technol. 2009, 43:1128-1133.
16. Girones R., Ferrús M.A., Alonso J.L., Manzano-Rodriguez J., Caluga B., Corrêa Ade A., Hundesa A., Carratula A., Bofil-Mas S. Molecular detection of pathogens in water - the pros and cons of molecular techniques. Water Res. 2010, 44:4325-4339.
17. Glassmeyer S.T., Furlong E.T., Kolpin D.W., Cahill J.D., Zaugg S.D., Werner S.L., Meyer M.T., Kryak D.D. Transport of chemical and microbial compounds from known wastewater discharges: potential for use as indicators of human fecal contamination. Environ. Sci. Technol. 2005, 39:5157-5169.
18. 2d) in Shiga toxigenic Escherichia coli from livestock sources. J. Clin. Microbiol. 2003, 41:3777-3783.
19. Graymore M., Stagnitti F., Allinson G. Impacts of atrazine in aquatic ecosystems. Environ. Int. 2001, 26:483-495.
20. Gyles C.L. Shiga toxin-producing Escherichia coli: an overview. J. Anim. Sci. 2007, 85(E. Suppl.):E45-E62.
21. Haack S.K. Antibiotic, Pharmaceutical, and Wastewater-compound Data for Michigan, 1998-2005. U.S. Geological Survey Scientific Investigations Report 2009-5217, U.S. Geological Survey, Reston, VA 2009.
22. Haack S.K., Duris J.W., Fogarty L.R., Kolpin D.W., Focazio M.J., Furlong E.T., Meyer M.T. Comparing wastewater chemicals, indicator bacteria concentrations, and bacterial pathogen genes as fecal pollution indicators. J. Environ. Qual. 2009, 38:248-258.
23. Hamelin K., Bruant G., El-Shaarawi A., Hill S., Edge T.A., Bekal S., Fairbrother J.M., Haerl J., Maynard C., Masson L., Brousseau R. A virulence and antimicrobial resistance DNA microarray detects a high frequency of virulence genes in Escherichia coli isolates from Great Lakes recreational waters. Appl. Environ. Microbiol. 2006, 72:4200-4206.
24. Helm P.A., Howell E.T., Li H., Metcalfe T.L., Chomicki K.M., Metcalfe C.D. Influence of nearshore dynamics on the distribution of organic waste-associated chemicals in Lake Ontario determined using passive samplers. J. Great Lakes Res. 2012, accessed at, (on Sept. 28, 2012). 10.1016/j.jglr.2012.01.005.
25. Herdendorf C.F. Great Lakes estuaries. Estuaries 1990, 13:493-503.
26. Higgins S.N., Pennuto C.M., Howell E.T., Lewis T., Makarewicz J.C. Urban influences on Cladophora blooms in Lake Ontario. J. Great Lakes Res. 2012, accessed at, (on Sept. 28, 2012). 10.1016/j/jglr.2011.12.005.
27. Howell E.T., Chomicki K.M., Kaltenecker G. Patterns in water quality on Canadian shores of Lake Ontario: correspondence with proximity to land and level of urbanization. J. Great Lakes Res. 2012, accessed at, (on Sept. 28, 2012). 10.1016/j/jglr.2011.11.017.
28. Hua W.Y., Bennett E.R., Maio X.S., Metcalfe C.D., Letcher R.J. Seasonality effects on pharmaceuticals and s-triazine herbicides in wastewater effluent and surface water from the Canadian side of the upper Detroit River. Environ. Toxicol. Chem. 2006, 25:2356-2365.
29. IJC (International Joint Commission) 15th Biennial Report 2012, International Joint Commission, Windsor, Ontario.
30. Indiana Department of Environmental Management Little Calumet River Watershed management plan accessed at, (on Sept. 28, 2012). http://ai.org/idem/nps/3228.htm.
31. Ishii S., Ksoll W.B., Hicks R.E., Sadowsky M.J. Presence and growth of naturalized Escherichia coli in temperate soils from Lake Superior watersheds. Appl. Environ. Microbiol. 2006, 72:612-621.
32. Jamieson R., Gordon R., Joy D., Lee H. Assessing microbial pollution of rural surface waters: a review of current watershed scale approaches. Agric. Water Manag. 2004, 70:1-17.
33. Jenkins T.M., Scott T.M., Morgan M.R., Rose J.B. Occurrence of alternative fecal indicators and enteric viruses in Michigan rivers. J. Great Lakes Res. 2005, 31:22-31.
34. Jofre J., Blanch A.R. Feasibility of methods based on nucleic acid amplification techniques to fulfill the requirements for microbiological analysis of water quality. J. Appl. Microbiol. 2010, 109:1853-1867.
35. Kim J.-W., Pachepsky Y.A., Shelton D.R., Coppock C. Effect of streambed bacteria release on E. coli concentrations: monitoring and modeling with the modified SWAT. Ecol. Model. 2010, 221:1592-1604.
36. Kinzelman J., McLellan S.L., Amick A., Preedit J., Scopel C.O., Olapade O., Gradus S., Singh A., Sedmak G. Identification of human enteric pathogens in gull feces at southwestern Lake Michigan bathing beaches. Can. J. Microbiol. 2008, 54:1006-1015.
37. Kleinheinz G.T., McDermott C.M., Hughes S., Brown A. Effects of rainfall on E. coli concentrations at Door County, Wisconsin Beaches. Int. J. Microbiol. 2009, 10.1155/2009/876050.
38. Löffler D., Römbke J., Meller M., Ternes T.A. Environmental fate of pharmaceuticals in water/sediment systems. Environ. Sci. Technol. 2005, 39:5209-5218.
39. Lozano N., Rice C.P., Pagano J., Zintek L., Barber L.B., Murphy E.W., Nettesheim T., Minarik T., Schoenfuss H.L. Concentration of organic contaminants in fish and their biological effects in a wastewater-dominated urban stream. Sci. Total. Environ. 2012, 420:191-201.
40. Mackey S. Nearshore physical processes. State of the Lakes Ecosystem Conference Background Paper 2008: Nearshore Areas of the Great Lakes 2009, 108-112. U.S. Environmental Protection Agency, Office of Water, Washington, D.C., (EPA 905-R-09-013).
41. Makarewicz J.C., Howell E.T. The Lake Ontario nearshore study: introduction and summary. J. Great Lakes Res. 2012, accessed at, (on Sept. 28, 2012). 10.1016/j/jglr.2012.07.006.
42. Metcalfe C.D., Miao X.S., Koenig B.G., Struger J. Distribution of acidic and neutral drugs in surface waters near sewage treatment plants in the lower Great Lakes, Canada. Environ. Toxicol. Chem. 2003, 22:2881-2889.
43. Nevers M.B., Whitman R.L. Nowcast modeling of Escherichia coli concentrations at multiple urban beaches of southern Lake Michigan. Water Res. 2005, 39:5250-5260.
44. Nevers M.B., Whitman R.L. Coastal strategies to predict Escherichia coli concentrations for beaches along a 35km stretch of southern Lake Michigan. Environ. Sci. Technol. 2008, 42:4454-4460.
45. New and Associates, J.F. Coffee Creek Watershed Management Plan 2003, J.F. New and Associates, Walkerton, IN, (accessed at http://www.coffeecreekwc.org/media/mgmt_plan_docs/mgmt_plan_web.pdf on Sept. 28, 2012).
46. NOAA (National Oceanic, Atmospheric Administration) Great Lakes Coastal Forecasting System: Indiana Dunes Nowcast Accessed at, (on Sept. 28, 2012). http://www.glerl.noaa.gov/res/glcfs/bd/.
47. Northwestern Indiana Regional Planning Commission Watershed Management Plan for Lake, Porter, and LaPorte Counties Accessed at, (on Sept. 28, 2012). http://www.nirpc.org/environment/pdf/Watershed%20Plan.pdf.
48. Oetken M., Nentwig G., Löffler D., Ternes T., Oehlmann J. Effects of pharmaceuticals on aquatic invertebrates. Part I. The antiepileptic drug carbamazepine. Arch. Environ. Contam. Toxicol. 2005, 49:353-361.
49. Patz J.A., Vavrus S.J., Uejio C.K., McLellan S.L. Climate change and waterborne disease risk in the Great Lakes region of the U.S. Am. J. Prev. Med. 2008, 35:451-458.
50. Peck A.M., Hornbuckle K. Environmental sources, occurrence, and effects of synthetic musk fragrances. J. Environ. Monit. 2006, 8:874-879.
51. Prager R., Fruth A., Siewert U., Strutz U., Tschape H. Escherichia coli encoding Shiga toxin 2f as an emerging human pathogen. Int. J. Med. Microbiol. 2009, 299:343-353.
52. Rao Y.R., Schwab D.J. Transport and mixing between the coastal and offshore waters in the Great Lakes: a review. J. Great Lakes Res. 2007, 33:202-218.
53. Savichtcheva O., Okayama N., Okabe S. Relationships between Bacteroides 16S rRNA genetic markers and presence of bacterial enteric pathogens and conventional fecal indicators. Water Res. 2007, 41:3615-3628.
54. Scopel C.O., Harris J., McLellan S.L. Influence of nearshore water dynamics and pollution sources on beach monitoring outcomes at two adjacent Lake Michigan beaches. J. Great Lakes Res. 2006, 32:543-552.
55. Thupaki P., Phanikumar M., Beletsky D., Schwab D.J., Nevers M., Whitman R.L. Budget analysis of Escherichia coli at a Southern Lake Michigan Beach. Environ. Sci. Technol. 2010, 44:1010-1016.
56. Twiss M.R., Marshall N.F. Tributary impacts on nearshore surface water quality detected during a late summer circumnavigation along the 20m isopleth of Lake Ontario. J. Great Lakes Res. 2012, accessed at, (on Sept. 28, 2012). 10.1016/j/jglr.2012.02.012.
57. USEPA (United States Environmental Protection Agency) Protocol for Developing Pathogen TMDLs 2001, United States Environmental Protection Agency, Office of Water, Washington, D.C., EPA 841-R-00-002. (Accessed on Sept. 28, 2012).
58. USEPA (United States Environmental Protection Agency) Quality Assurance/quality Control Guidance for Laboratories Performing PCR Analyses on Environmental Samples 2004, United States Environmental Protection Agency, Office of Water, Washington, D.C, (EPA 815-B-04-001).
59. USEPA (United States Environmental Protection Agency) Ambient Aquatic Life Water Quality Criteria-nonylphenol Final 2005, Office of Water, Office of Science and Technology, Washington, DC, (EPA-822-R-05-005).
60. USEPA (United States Environmental Protection Agency) Watershed Assessment, Tracking & Environmental ResultS (WATERS) Database, Indiana Water Quality Assessment Report accessed at, (on Sept. 28, 2012). http://iaspub.epa.gov/tmdl_waters10/attains_state.control?p_state=IN&p_cycle=2006.
61. USEPA (United States Environmental Protection Agency) Recreational Water Quality Criteria 2012, Office of Water, Washington, D.C, (EPA-820-F-12-058, 63 pp., accessed at http://water.epa.gov/scitech/swguidance/standards/criteria/health/recreation/index.cfm on Dec. 15, 2012).
62. USGS (United States Geological Survey) Water-resources data for the United States, Water Year 2011: U.S. Geological Survey Water-Data Report WDR-US-2011, site 04095090 accessed at, (on Sept. 28, 2012). http://wdr.water.usgs.gov/wy2011/pdfs/04095090.2011.pdf.
63. Uslu M.O., Biswas N., Jasim S. Chemicals of Emerging Concern in the Great Lakes Region 2012, International Joint Commission, Windsor, Ontario, Canada, (IJC Report ID 696. Accessed at http://www.ijc.org/php/publications/pdf/ID696.pdf on Sept. 28, 2012).
64. Whitman R.L., Przybyla-Kelly K., Shiveky D.A., Byappanahalli M.N. Incidence of the enterococcal surface protein (esp) gene in human and animal fecal sources. Environ. Sci. Technol. 2007, 41:6090-6095.
65. Wilkes G., Edge T., Gannon V., Jokinen C., Lyautey E., Medeiros D., Neumann N., Ruecker N., Topp E., Lapen D.R. Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural landscape. Water Res. 2009, 43:2209-2223.
66. Wittman, Hydro Planning Associates Inc Salt Creek E. coli TMDL 2004, Wittman Hydro Planning Associates, Inc, Bloomington, IN, (accessed at http://www.epa.gov/waters/tmdldocs/salt%20creek%20e%20coli%20final%20tmdl%20report.pdf on Sept. 28, 2012).
67. Wong M., Kumar L., Jenkins T.M., Xagoraraki I., Phanikumar M.S., Rose J.B. Evaluation of public health risks at recreational beaches in Lake Michigan via detection of enteric viruses and a human-specific bacteriological markers. Water Res. 2009, 43:1137-1149.
68. Xagoraraki I., Kuo D.H.-W., Wong K., Wong M., Rose J.B. Occurrence of human adenoviruses at two recreational beaches of the Great Lakes. Appl. Environ. Microbiol. 2007, 73:7874-7881.
69. Zaugg S.D., Smith S.G., Schroeder M.l P., Barber L.B., Burkhardt M.R. Methods of Analysis by the U.S. Geological Survey National Water Quality Laboratory - Determination of Wastewater Compounds by Polystyrene-Divinylbenzene Solid-Phase Extraction and Capillary-Column Gas Chromatography/Mass Spectrometry. USGS Water-Resources Investigations Report 2001-4186 2002, U.S. Geological Survey, Reston, VA.
70. Ziebell K.A., Read S.C., Johnson R.P., Gyles C.L. Evaluation of PCR and PCR-RFLP protocols for identifying shiga toxins. Res. Microbiol. 2002, 153:289-300.