The Microcosm Mediates the Persistence of Shiga Toxin-Producing Escherichia coli in Freshwater Ecosystems

ABSTRACT Water is a major route for infection of humans by exotoxin-producing bacteria, including Shiga toxin-producing Escherichia coli (STEC). While STEC has the potential to be present in nearly every type of water source, its distribution is sporadic, and an understanding of factors that govern its emergence and persistence within water is lacking. In this study, we examined the influence of microbe content on STEC persistence in freshwater. We found that depletion of microbes in the water leads to a considerable increase in the persistence of STEC, an effect that can be mitigated by adding grazing protists to the water. STEC strains appear to be more resistant to the impact of grazing protists than E. coli strains that lack the Shiga toxin (stx) gene. Our results demonstrate that the microcosm can dramatically influence the persistence of STEC in aquatic ecosystems and that the overall impact by microbes on STEC strains is fundamentally different from that of non-STEC strains of bacteria. Overall, these results provide insight into why STEC and possibly other exotoxin-producing bacterial pathogens display such variability in abundance, distribution, and persistence in aquatic ecosystems.

[1]  Y. Tsai,et al.  Occurrence of Genes Associated with Enterotoxigenic and Enterohemorrhagic Escherichia coli in Agricultural Waste Lagoons , 2004, Applied and Environmental Microbiology.

[2]  J. Lim,et al.  Involvement of the Escherichia coli O157:H7(pO157) ecf Operon and Lipid A Myristoyl Transferase Activity in Bacterial Survival in the Bovine Gastrointestinal Tract and Bacterial Persistence in Farm Water Troughs , 2005, Infection and Immunity.

[3]  T. Honda.  [Bacterial protein toxins]. , 1999, Nihon rinsho. Japanese journal of clinical medicine.

[4]  J. Rothberg,et al.  Prospective Genomic Characterization of the German Enterohemorrhagic Escherichia coli O104:H4 Outbreak by Rapid Next Generation Sequencing Technology , 2011, PloS one.

[5]  A. O’Brien,et al.  Activation of Shiga-like toxins by mouse and human intestinal mucus correlates with virulence of enterohemorrhagic Escherichia coli O91:H21 isolates in orally infected, streptomycin-treated mice , 1996, Infection and immunity.

[6]  G. Koudelka,et al.  Entry and Killing of Tetrahymena thermophila by Bacterially Produced Shiga Toxin , 2012, mBio.

[7]  G. Koudelka,et al.  Shiga Toxin: Expression, Distribution, and Its Role in the Environment , 2011, Toxins.

[8]  A. Weiss,et al.  Shiga Toxin Subtypes Display Dramatic Differences in Potency , 2011, Infection and Immunity.

[9]  A. Ibekwe,et al.  Multiplex Fluorogenic Real-Time PCR for Detection and Quantification of Escherichia coli O157:H7 in Dairy Wastewater Wetlands , 2002, Applied and Environmental Microbiology.

[10]  M. Breitbart,et al.  Widespread occurrence of phage-encoded exotoxin genes in terrestrial and aquatic environments in Southern California. , 2006, FEMS microbiology letters.

[11]  C. Gyles.  Shiga toxin-producing Escherichia coli: an overview. , 2007, Journal of animal science.

[12]  P. Younger,et al.  Stedman's Medical Dictionary, 28th ed. , 2007 .

[13]  J. Jofre,et al.  Occurrence of phages infecting Escherichia coli O157:H7 carrying the Stx 2 gene in sewage from different countries. , 2000, FEMS microbiology letters.

[14]  M. Muniesa,et al.  Characterizing RecA-Independent Induction of Shiga toxin2-Encoding Phages by EDTA Treatment , 2012, PloS one.

[15]  L. Mcdaniel,et al.  Effect of Nutrient Addition and Environmental Factors on Prophage Induction in Natural Populations of Marine Synechococcus Species , 2005, Applied and Environmental Microbiology.

[16]  U. Obst,et al.  Application of the fluorogenic probe technique (TaqMan PCR) to the detection of Enterococcus spp. and Escherichia coli in water samples. , 2003, Journal of microbiological methods.

[17]  S. Wai,et al.  A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Hadler,et al.  Hemolytic-Uremic Syndrome and Escherichia coli O121 at a Lake in Connecticut, 1999. , 2001, Pediatrics.

[19]  J. Livny,et al.  Lambdoid Phages and Shiga Toxin , 2005 .

[20]  M. Krönke,et al.  Therapeutic concentrations of antibiotics inhibit Shiga toxin release from enterohemorrhagic E. coli O104:H4 from the 2011 German outbreak , 2012, BMC Microbiology.

[21]  G. Koudelka,et al.  Shiga Toxin as a Bacterial Defense against a Eukaryotic Predator, Tetrahymena thermophila , 2009, Journal of bacteriology.

[22]  H. Livingstone.  STEDMAN'S MEDICAL DICTIONARY , 1961, The Ulster Medical Journal.

[23]  David L. Swerdlow,et al.  Epidemiology of Escherichia coli O157:H7 Outbreaks, United States, 1982–2002 , 2005, Emerging infectious diseases.

[24]  John F. Griffith,et al.  Comparison of Rapid Quantitative PCR-Based and Conventional Culture-Based Methods for Enumeration of Enterococcus spp. and Escherichia coli in Recreational Waters , 2010, Applied and Environmental Microbiology.

[25]  A. Thebo,et al.  Impact of urbanization and agriculture on the occurrence of bacterial pathogens and stx genes in coastal waterbodies of central California. , 2011, Water research.

[26]  J. Gunderson,et al.  Interactions between Food-Borne Pathogens and Protozoa Isolated from Lettuce and Spinach , 2008, Applied and Environmental Microbiology.

[27]  J. Jofre,et al.  Detection, enumeration and isolation of strains carrying the stx2 gene from urban sewage. , 2003, Water science and technology : a journal of the International Association on Water Pollution Research.

[28]  T. Hindré,et al.  Shiga toxin produced by enterohemorrhagic Escherichia coli inhibits PI3K/NF-κB signaling pathway in globotriaosylceramide-3-negative human intestinal epithelial cells. , 2008, The Journal of Immunology.

[29]  C. Saelinger.  Receptors for Bacterial Toxins , 2003 .

[30]  Correlation of Shiga Toxin Gene Frequency with Commonly Used Microbial Indicators of Recreational Water Quality , 2008, Applied and Environmental Microbiology.

[31]  T. Hindré,et al.  Shiga Toxin Produced by Enterohemorrhagic Escherichia coli Inhibits PI3K/NF-κB Signaling Pathway in Globotriaosylceramide-3-Negative Human Intestinal Epithelial Cells1 , 2007, The Journal of Immunology.

[32]  Awwa,et al.  Standard Methods for the examination of water and wastewater , 1999 .

[33]  A. Blanch,et al.  Occurrence of Escherichia coli O157:H7 and other enterohemorrhagic Escherichia coli in the environment. , 2006, Environmental science & technology.

[34]  R. Holmes,et al.  Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. , 1984, Science.

[35]  A. E. Greenberg,et al.  Standard methods for the examination of water and wastewater : supplement to the sixteenth edition , 1988 .