Microbial Ecology

, Volume 62, Issue 3, pp 574–583 | Cite as

Terrestrial Sources Homogenize Bacterial Water Quality During Rainfall in Two Urbanized Watersheds in Santa Barbara, CA

  • Bram Sercu
  • Laurie C. Van De Werfhorst
  • Jill L. S. Murray
  • Patricia A. Holden
Environmental Microbiology


Microbiological contamination from runoff is a human health concern in urbanized coastal environments, but the contamination sources are often unknown. This study quantified fecal indicator bacteria and compared the distributions of human-specific genetic markers and bacterial community composition during dry and wet weather in urban creeks draining two neighboring watersheds in Santa Barbara, CA. In a prior study conducted during exclusively dry weather, the creeks were contaminated with human waste as indicated by elevated numbers of the human-specific Bacteroidales marker HF183 (Sercu et al. in Environ Sci Technol 43:293–298, 2009). During the storm, fecal indicator bacterial numbers and loads increased orders of magnitude above dry weather conditions. Moreover, bacterial community composition drastically changed during rainfall and differed from dry weather flow by (1) increased bacterial diversity, (2) reduced spatial heterogeneity within and between watersheds, and (3) clone library sequences more related to terrestrial than freshwater taxa. Finally, the spatial patterns of human-associated genetic markers (HF183 and Methanobrevibacter smithii nifH gene) changed during wet weather, and the contribution of surface soils to M. smithii nifH gene detection was suspected. The increased fecal indicator bacteria numbers during wet weather were likely associated with terrestrial sources, instead of human waste sources that dominated during dry weather flow.


Terminal Restriction Fragment Length Polymorphism Bacterial Community Composition nifH Gene Fecal Indicator Bacterium Terminal Restriction Fragment Length Polymorphism Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This research was supported by the City of Santa Barbara through Measure B funding and by the Switzer Foundation through a Leadership Grant to the City. Flow data were provided through the NSF-funded Santa Barbara Long Term Ecological Research project (NSF OCE 9982105 and OCE 0620276) with assistance from Scott Coombs, Blair Goodridge, and John Melack. Additional assistance at UCSB was from Shurong Xiang, Allison Horst and John Priester (for sampling and sample processing), and Noah Fierer (clone library analysis). Additional assistance from the City of Santa Barbara was from Tim Burgess, Jill Zachary, Harry Slicker, Steve Mack, and Rebecca Bjork.

Supplementary material

248_2011_9874_MOESM1_ESM.doc (400 kb)
ESM 1 (DOC 400 kb)


  1. 1.
    Ahmed W, Goonetilleke A, Powell D, Chauhan K, Gardner T (2009) Comparison of molecular markers to detect fresh sewage in environmental waters. Water Res 43:4908–4917PubMedCrossRefGoogle Scholar
  2. 2.
    Ahmed W, Stewart J, Gardner T, Powell D, Brooks P, Sullivana D, Tindale N (2007) Sourcing faecal pollution: a combination of library-dependent and library-independent methods to identify human faecal pollution in non-sewered catchments. Water Res 41:3771–3779PubMedCrossRefGoogle Scholar
  3. 3.
    Ahn JH, Grant SB, Surbeck CQ, Digiacomo PM, Nezlin NP, Jiang S (2005) Coastal water quality impact of stormwater runoff from an urban watershed in southern California. Environ Sci Technol 39:5940–5953PubMedCrossRefGoogle Scholar
  4. 4.
    Balbus JM, Embrey MA (2002) Risk factors for waterborne enteric infections. Curr Opin Gastroenterol 18:46–50PubMedCrossRefGoogle Scholar
  5. 5.
    Brownell MJ, Harwood VJ, Kurz RC, McQuaig SM, Lukasik J, Scott TM (2007) Confirmation of putative stormwater impact on water quality at a Florida beach by microbial source tracking methods and structure of indicator organism populations. Water Res 41:3747–3757PubMedCrossRefGoogle Scholar
  6. 6.
    Choi S, Jiang SC (2005) Real-time PCR quantification of human adenoviruses in urban rivers indicates genome prevalence but low infectivity. Appl Environ Microbiol 71:7426–7433PubMedCrossRefGoogle Scholar
  7. 7.
    City of Santa Barbara (2005) Existing conditions study of the Arroyo Burro, Mission, Sycamore, and Laguna creek watersheds. Creeks Restoration and Water Quality Improvement Division, Santa BarbaraGoogle Scholar
  8. 8.
    Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E, PlymouthGoogle Scholar
  9. 9.
    Crump BC, Hobbie JE (2005) Synchrony and seasonality in bacterioplankton communities of two temperate rivers. Limnol Oceanogr 50:1718–1729CrossRefGoogle Scholar
  10. 10.
    Harwood VJ, Brownell M, Wang S, Lepo J, Ellender RD, Ajidahun A, Hellein KN, Kennedy E, Ye XY, Flood C (2009) Validation and field testing of library-independent microbial source tracking methods in the Gulf of Mexico. Water Res 43:4812–4819PubMedCrossRefGoogle Scholar
  11. 11.
    Ishii S, Sadowsky MJ (2008) Escherichia coli in the environment: implications for water quality and human health. Microbes Environ 23:101–108PubMedCrossRefGoogle Scholar
  12. 12.
    Jiang SC, Chu W, Olson BH, He JW, Choi S, Zhang J, Le JY, Gedalanga PB (2007) Microbial source tracking in a small southern California urban watershed indicates wild animals and growth as the source of fecal bacteria. Appl Microbiol Biotechnol 76:927–934PubMedCrossRefGoogle Scholar
  13. 13.
    Kemp PF, Aller JY (2004) Estimating prokaryotic diversity: when are 16S rDNA libraries large enough? Limnol Oceanogr-Methods 2:114–125CrossRefGoogle Scholar
  14. 14.
    Kildare BJ, Leutenegger CM, McSwain BS, Bambic DG, Rajal VB, Wuertz S (2007) 16S rRNA-based assays for quantitative detection of universal, human-, cow-, and dog-specific fecal Bacteroidales: a Bayesian approach. Water Res 41:3701–3715PubMedCrossRefGoogle Scholar
  15. 15.
    Krometis LAH, Characklis GW, Simmons OD, Dilts MJ, Likirdopulos CA, Sobsey MD (2007) Intra-storm variability in microbial partitioning and microbial loading rates. Water Res 41:506–516PubMedCrossRefGoogle Scholar
  16. 16.
    LaMontagne MG, Holden PA (2003) Comparison of free-living and particle-associated bacterial communities in a coastal lagoon. Microb Ecol 46:228–237PubMedCrossRefGoogle Scholar
  17. 17.
    Mackenzie WR, Hoxie NJ, Proctor ME, Gradus MS, Blair KA, Peterson DE, Kazmierczak JJ, Addiss DG, Fox KR, Rose JB, Davis JP (1994) A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. New Engl J Med 331:161–167CrossRefGoogle Scholar
  18. 18.
    Mallin MA, Johnson VL, Ensign SH (2009) Comparative impacts of stormwater runoff on water quality of an urban, a suburban, and a rural stream. Environ Monit Assess 159:475–491PubMedCrossRefGoogle Scholar
  19. 19.
    McCarthy DT (2009) A traditional first flush assessment of E. coli in urban stormwater runoff. Water Sci Technol 60:2749–2757PubMedCrossRefGoogle Scholar
  20. 20.
    Morrison CR, Bachoon DS, Gates KW (2008) Quantification of enterococci and bifidobacteria in Georgia estuaries using conventional and molecular methods. Water Res 42:4001–4009PubMedCrossRefGoogle Scholar
  21. 21.
    Nautiyal CS, Rehman A, Chauhan PS (2010) Environmental Escherichia coli occur as natural plant growth-promoting soil bacterium. Arch Microbiol 192:185–193PubMedCrossRefGoogle Scholar
  22. 22.
    Noble RT, Griffith JF, Blackwood AD, Fuhrman JA, Gregory JB, Hernandez X, Liang XL, Bera AA, Schiff K (2006) Multitiered approach using quantitative PCR to track sources of fecal pollution affecting Santa Monica Bay, California. Appl Environ Microbiol 72:1604–1612PubMedCrossRefGoogle Scholar
  23. 23.
    Peters NE (2009) Effects of urbanization on stream water quality in the city of Atlanta, Georgia, USA. Hydrol Process 23:2860–2878CrossRefGoogle Scholar
  24. 24.
    Rajal VB, McSwain BS, Thompson DE, Leutenegger CM, Wuertz S (2007) Molecular quantitative analysis of human viruses in California stormwater. Water Res 41:4287–4298PubMedCrossRefGoogle Scholar
  25. 25.
    Reeves RL, Grant SB, Mrse RD, Oancea CMC, Sanders BF, Boehm AB (2004) Scaling and management of fecal indicator bacteria in runoff from a coastal urban watershed in southern California. Environ Sci Technol 38:2637–2648PubMedCrossRefGoogle Scholar
  26. 26.
    Roslev P, Bukh AS (2011) State of the art molecular markers for fecal pollution source tracking in water. Appl Microbiol Biotechnol 89:1341–1355PubMedCrossRefGoogle Scholar
  27. 27.
    Savichtcheva O, Okayama N, Okabe S (2007) Relationships between Bacteroides 16S rRNA genetic markers and presence of bacterial enteric pathogens and conventional fecal indicators. Water Res 41:3615–3628PubMedCrossRefGoogle Scholar
  28. 28.
    Schriewer A, Miller WA, Byrne BA, Miller MA, Oates S, Conrad PA, Hardin D, Yang HH, Chouicha N, Melli A, Jessup D, Dominik C, Wuertz S (2010) Presence of Bacteroidales as a predictor of pathogens in surface waters of the central California coast. Appl Environ Microbiol 76:5802–5814PubMedCrossRefGoogle Scholar
  29. 29.
    Sercu B, Van De Werfhorst LC, Murray J, Holden PA (2009) Storm drains are sources of human fecal pollution during dry weather in three urban Southern California watersheds. Environ Sci Technol 43:293–298PubMedCrossRefGoogle Scholar
  30. 30.
    Sercu B, Van De Werfhorst LC, Murray J, Holden PA (2011) Cultivation-independent analysis of bacteria in IDEXX Quanti-Tray/2000 fecal indicator assays. Appl Environ Microbiol 77:627–633PubMedCrossRefGoogle Scholar
  31. 31.
    Seurinck S, Defoirdt T, Verstraete W, Siciliano SD (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 7:249–259PubMedCrossRefGoogle Scholar
  32. 32.
    Shehane SD, Harwood VJ, Whitlock JE, Rose JB (2005) The influence of rainfall on the incidence of microbial faecal indicators and the dominant sources of faecal pollution in a Florida river. J Appl Microbiol 98:1127–1136PubMedCrossRefGoogle Scholar
  33. 33.
    Soller JA, Schoen ME, Bartrand T, Ravenscroft JE, Ashbolt J (2010) Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Res 44:4674–4691PubMedCrossRefGoogle Scholar
  34. 34.
    Solo-Gabriele HM, Wolfert MA, Desmarais TR, Palmer CJ (2000) Sources of Escherichia coli in a coastal subtropical environment. Appl Environ Microbiol 66:230–237PubMedCrossRefGoogle Scholar
  35. 35.
    Sullivan TJ, Snyder KU, Gilbert E, Bischoff JM, Wustenberg M, Moore J, Moore D (2005) Assessment of water quality in association with land use in the Tillamook Bay Watershed, Oregon, USA. Water Air Soil Pollut 161:3–23CrossRefGoogle Scholar
  36. 36.
    Surbeck CQ, Jiang SC, Ahn JH, Grant SB (2006) Flow fingerprinting fecal pollution and suspended solids in stormwater runoff from an urban coastal watershed. Environ Sci Technol 40:4435–4441PubMedCrossRefGoogle Scholar
  37. 37.
    Tholen A, Pester M, Brune A (2007) Simultaneous methanogenesis and oxygen reduction by Methanobrevibacter cuticularis at low oxygen fluxes. FEMS Microbiol Ecol 62:303–312PubMedCrossRefGoogle Scholar
  38. 38.
    Ufnar JA, Wang SY, Christiansen JM, Yampara-Iquise H, Carson CA, Ellender RD (2006) Detection of the nifH gene of Methanobrevibacter smithii: a potential tool to identify sewage pollution in recreational waters. J Appl Microbiol 101:44–52PubMedCrossRefGoogle Scholar
  39. 39.
    Verhougstraete MP, Byappanahalli MN, Rose JB, Whitman RL (2010) Cladophora in the Great Lakes: impacts on beach water quality and human health. Water Sci Technol 62:68–76PubMedCrossRefGoogle Scholar
  40. 40.
    Walters SP, Gannon VPJ, Field KG (2007) Detection of Bacteroidales fecal indicators and the zoonotic pathogens E. coli O157:H7, Salmonella, and Campylobacter in river water. Environ Sci Technol 41:1856–1862PubMedCrossRefGoogle Scholar
  41. 41.
    Walters SP, Field KG (2009) Survival and persistence of human and ruminant-specific faecal Bacteroidales in freshwater microcosms. Environ Microbiol 11:1410–1421PubMedCrossRefGoogle Scholar
  42. 42.
    Walters SP, Yamahara KM, Boehm AB (2009) Persistence of nucleic acid markers of health-relevant organisms in seawater microcosms: implications for their use in assessing risk in recreational waters. Water Res 43:4929–4939PubMedCrossRefGoogle Scholar
  43. 43.
    Warnecke F, Amann R, Pernthaler J (2004) Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environ Microbiol 6:242–253PubMedCrossRefGoogle Scholar
  44. 44.
    Wu X, Xi W, Ye W, Yang H (2007) Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiol Ecol 61:85–96PubMedCrossRefGoogle Scholar
  45. 45.
    Yamahara KM, Walters S, Boehm AB (2009) Growth of enterococci in unaltered unseeded beach sands subjected to tidal wetting. Appl Environ Microbiol 75:1517–1524PubMedCrossRefGoogle Scholar
  46. 46.
    Zwart G, Crump BC, Agterveld M, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Bram Sercu
    • 1
    • 2
  • Laurie C. Van De Werfhorst
    • 1
    • 2
  • Jill L. S. Murray
    • 3
  • Patricia A. Holden
    • 1
    • 2
  1. 1.Donald Bren School of Environmental Science and ManagementUniversity of CaliforniaSanta BarbaraUSA
  2. 2.Earth Research InstituteUniversity of CaliforniaSanta BarbaraUSA
  3. 3.City of Santa Barbara, Creeks Restoration and Water Quality Improvement DivisionSanta BarbaraUSA

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