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      Suppression of Escherichia coli O157:H7 by Dung Beetles (Coleoptera: Scarabaeidae) Using the Lowbush Blueberry Agroecosystem as a Model System

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          Abstract

          Wildlife as a source of microbial contamination is a food safety concern. Deer feces (scat) have been determined as a point source for Escherichia coli O157:H7 contamination of fresh produce. The ecological role of the scooped scarab ( Onthophagus hecate (Panzer)), a generalist dung beetle species common in Maine blueberry fields, was explored as a biological control agent and alternatively as a pathogen vector between deer scat and food.

          A large-scale field survey of wildlife scat indicated that pathogenic E. coli O157:H7 was present, albeit at a low prevalence (1.9% of samples, n = 318), in the Maine lowbush blueberry agroecosystem. A manipulative field experiment verified that, should contact occur between deer scat and blueberry plants and fruit during the summer, contamination with E. coli O157:H7 can occur and persist for more than 72 h. For both the positive control and an experimental scat inoculation treatment, the levels of the bacterial population decreased over time, but at different rates (treatment x time interaction: F (1.9,18.8) = 358.486, P < 0.0001). The positive control inoculation, which resulted in a higher initial E. coli level on fruit, decayed at a faster rate than inoculation of fruit via scat in the experimental treatment.

          We conducted 2 laboratory studies to elucidate aspects of dung beetle feeding ecology as it relates to suppression of E. coli O157:H7 from deer scat to lowbush blueberry fruit. In both experiments, dung beetles buried the same amount of scat whether or not the scat was inoculated with the pathogen ( F (1,6) = 0.001; P = 0.999 and ( F (2,17) = 4.10, P = 0.147). Beetles feeding on E. coli inoculated deer scat were not found to vector the pathogen to fruit. In two studies, beetles lowered the amount of pathogenic E. coli persisting in soils compared to soils without beetles ( F (2,9) = 7.757; P = 0.05 and F (2,17) = 8.0621, P = 0.004).

          Our study suggests that the dung beetle species, Onthophagus hecate, has the potential to contribute to the suppression of E. coli O157:H7 in agricultural landscapes.

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          Escherichia coli O157:H7: animal reservoir and sources of human infection.

          This review surveys the literature on carriage and transmission of enterohemorrhagic Escherichia coli (EHEC) O157:H7 in the context of virulence factors and sampling/culture technique. EHEC of the O157:H7 serotype are worldwide zoonotic pathogens responsible for the majority of severe cases of human EHEC disease. EHEC O157:H7 strains are carried primarily by healthy cattle and other ruminants, but most of the bovine strains are not transmitted to people, and do not exhibit virulence factors associated with human disease. Prevalence of EHEC O157:H7 is probably underestimated. Carriage of EHEC O157:H7 by individual animals is typically short-lived, but pen and farm prevalence of specific isolates may extend for months or years and some carriers, designated as supershedders, may harbor high intestinal numbers of the pathogen for extended periods. The prevalence of EHEC O157:H7 in cattle peaks in the summer and is higher in postweaned calves and heifers than in younger and older animals. Virulent strains of EHEC O157:H7 are rarely harbored by pigs or chickens, but are found in turkeys. The bacteria rarely occur in wildlife with the exception of deer and are only sporadically carried by domestic animals and synanthropic rodents and birds. EHEC O157:H7 occur in amphibian, fish, and invertebrate carriers, and can colonize plant surfaces and tissues via attachment mechanisms different from those mediating intestinal attachment. Strains of EHEC O157:H7 exhibit high genetic variability but typically a small number of genetic types predominate in groups of cattle and a farm environment. Transmission to people occurs primarily via ingestion of inadequately processed contaminated food or water and less frequently through contact with manure, animals, or infected people. © Mary Ann Liebert, Inc.
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            Escherichia coli O157:H7 in Feral Swine near Spinach Fields and Cattle, Central California Coast1

            We investigated involvement of feral swine in contamination of agricultural fields and surface waterways with Escherichia coli O157:H7 after a nationwide outbreak traced to bagged spinach from California. Isolates from feral swine, cattle, surface water, sediment, and soil at 1 ranch were matched to the outbreak strain.
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              Dispersal and gene flow in free-living marine nematodes

              Dispersal and gene flow determine connectivity among populations, and can be studied through population genetics and phylogeography. We here review the results of such a framework for free-living marine nematodes. Although field experiments have illustrated substantial dispersal in nematodes at ecological time scales, analysis of the genetic diversity illustrated the importance of priority effects, founder effects and genetic bottlenecks for population structuring between patches <1 km apart. In contrast, only little genetic structuring was observed within an estuary (<50 km), indicating that these small scale fluctuations in genetic differentiation are stabilized over deeper time scales through extensive gene flow. Interestingly, nematode species with contrasting life histories (extreme colonizers vs persisters) or with different habitat preferences (algae vs sediment) show similar, low genetic structuring. Finally, historical events have shaped the genetic pattern of marine nematodes and show that gene flow is restricted at large geographical scales. We also discuss the presence of substantial cryptic diversity in marine nematodes, and end with highlighting future important steps to further unravel nematode evolution and diversity.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 April 2015
                2015
                : 10
                : 4
                : e0120904
                Affiliations
                [1 ]University of Maine, School of Biology and Ecology, Orono, ME, United States of America
                [2 ]Washington State University, Department of Entomology, Pullman, WA, United States of America
                [3 ]University of Maine, School of Food and Agriculture, Orono, ME, United States of America
                [4 ]University of Maine, Cooperative Extension, Orono, ME, United States of America
                USDA-ARS-ERRC, UNITED STATES
                Author notes

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

                Conceived and designed the experiments: MSJ ST VCHW FD. Performed the experiments: MSJ ST DFB. Analyzed the data: MSJ FD ST VCHW. Contributed reagents/materials/analysis tools: VCHW FD. Wrote the paper: MSJ ST VCHW FD. Set up and managed the overall project: MSJ ST DFB VCHW FD.

                ‡ VCHW and FD are joint senior authors on this work.

                Article
                PONE-D-14-41425
                10.1371/journal.pone.0120904
                4388438
                25849430
                a36758a4-91bf-46e8-96c4-485edd7231f8
                Copyright @ 2015

                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
                : 15 September 2014
                : 27 January 2015
                Page count
                Figures: 3, Tables: 0, Pages: 14
                Funding
                This research was supported by the Center for Produce Safety and the Maine Agricultural and Forest Experiment Station at the University of Maine with external publication number 3406. This work is based upon research supported in part by Hatch Grant number ME08562-10 from the USDA National Institute of Food and Agriculture. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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