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      Protozoan Predation of Escherichia coli O157:H7 Is Unaffected by the Carriage of Shiga Toxin-Encoding Bacteriophages

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          Abstract

          Escherichia coli O157:H7 is a food-borne bacterium that causes hemorrhagic diarrhea and hemolytic uremic syndrome in humans. While cattle are a known source of E. coli O157:H7 exposure resulting in human infection, environmental reservoirs may also be important sources of infection for both cattle and humans. Bacteriophage-encoded Shiga toxins (Stx) carried by E. coli O157:H7 may provide a selective advantage for survival of these bacteria in the environment, possibly through their toxic effects on grazing protozoa. To determine Stx effects on protozoan grazing, we co-cultured Paramecium caudatum, a common ciliate protozoon in cattle water sources, with multiple strains of Shiga-toxigenic E. coli O157:H7 and non-Shiga toxigenic cattle commensal E. coli. Over three days at ambient laboratory temperature, P. caudatum consistently reduced both E. coli O157:H7 and non-Shiga toxigenic E. coli populations by 1–3 log cfu. Furthermore, a wild-type strain of Shiga-toxigenic E. coli O157:H7 (EDL933) and isogenic mutants lacking the A subunit of Stx 2a, the entire Stx 2a-encoding bacteriophage, and/or the entire Stx 1-encoding bacteriophage were grazed with similar efficacy by both P. caudatum and Tetrahymena pyriformis (another ciliate protozoon). Therefore, our data provided no evidence of a protective effect of either Stx or the products of other bacteriophage genes on protozoan predation of E. coli. Further research is necessary to determine if the grazing activity of naturally-occurring protozoa in cattle water troughs can serve to decrease cattle exposure to E. coli O157:H7 and other Shiga-toxigenic E. coli.

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          Most cited references16

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          The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions.

          Polymerase chain reaction conditions were established for the in vitro amplification of eukaryotic small subunit ribosomal (16S-like) rRNA genes. Coding regions from algae, fungi, and protozoa were amplified from nanogram quantities of genomic DNA or recombinant plasmids containing rDNA genes. Oligodeoxynucleotides that are complementary to conserved regions at the 5' and 3' termini of eukaryotic 16S-like rRNAs were used to prime DNA synthesis in repetitive cycles of denaturation, reannealing, and DNA synthesis. The fidelity of synthesis for the amplification products was evaluated by comparisons with sequences of previously reported rRNA genes or with primer extension analyses of rRNAs. Fewer than one error per 2000 positions were observed in the amplified rRNA coding region sequences. The primary structure of the 16S-like rRNA from the marine diatom, Skeletonema costatum, was inferred from the sequence of its in vitro amplified coding region.
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            The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome.

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              Shiga toxin-associated hemolytic uremic syndrome: pathophysiology of endothelial dysfunction.

              Shiga toxin (Stx)-producing enterohemorrhagic Escherichia coli O157:H7 has become a global threat to public health, as a primary cause of a worldwide spread of hemorrhagic colitis complicated by diarrhea-associated hemolytic uremic syndrome (HUS), a disorder of thrombocytopenia, microangiopathic hemolytic anemia, and acute renal failure that mainly affects early childhood. Endothelial dysfunction has been recognized as the trigger event in the development of microangiopathic processes. Endothelial cells, mainly those located in the renal microvasculature, are primary targets of the toxic effects of Stx1 and 2. Stxs bound to their specific globotriaosylceramide (Gb3Cer) receptor on the cell surface trigger a cascade of signaling events, involving NF-κB activation, that induce expression of genes encoding for adhesion molecules and chemokines, and culminate in the adhesion of leukocytes to endothelial cells, thereby increasing the endothelial susceptibility to leukocyte-mediated injury. Activated endothelial cells in response to Stxs lose the normal thromboresistance phenotype and become thrombogenic, initiating microvascular thrombus formation. Evidence is emerging that complement activation in response to Stxs favors platelet thrombus formation on endothelial cells, which may play a role in amplifying the inflammation-thrombosis circuit in Stx-associated HUS.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                29 January 2016
                2016
                : 11
                : 1
                : e0147270
                Affiliations
                [001]Department of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, Washington, United States of America
                The Pennsylvania State University, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CES SS TEB. Performed the experiments: CES SS. Analyzed the data: CES TEB. Contributed reagents/materials/analysis tools: CES SS TEB. Wrote the paper: CES SS TEB.

                Article
                PONE-D-14-54265
                10.1371/journal.pone.0147270
                4732659
                26824472
                a94b2a08-c180-4a9c-a887-b50ee1f0d72c
                © 2016 Schmidt et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 3 December 2014
                : 25 December 2015
                Page count
                Figures: 4, Tables: 2, Pages: 11
                Funding
                This work was supported by Agriculture and Food Research Initiative competitive grant no. 2010-04487, from the USDA National Institute of Food and Agriculture, an NIH T32 Training Grant, and the ARCS Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Viruses
                Bacteriophages
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Mammals
                Bovines
                Cattle
                Biology and Life Sciences
                Agriculture
                Livestock
                Cattle
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Mammals
                Ruminants
                Cattle
                Biology and Life Sciences
                Organisms
                Protozoans
                Biology and Life Sciences
                Behavior
                Animal Behavior
                Grazing
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Grazing
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Escherichia Coli Infections
                Medicine and Health Sciences
                Parasitic Diseases
                Protozoan Infections
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Predation
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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                Uncategorized

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