Biofilm as an Environment for Dissemination of
            <i>stx</i>
            Genes by Transduction

Solheim, Heidi; Sekse, Camilla; Urdahl, Anne Margrete; Wasteson, Yngvild; Nesse, Live L.

doi:10.1128/aem.03512-12

Cited by 47 publications

(38 citation statements)

References 27 publications

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“…The lysogens in our experiments were selected by antibiotics to facilitate the detection on the agar plates, and lower frequencies would probably be obtained without selection, but it should be noted that the lysogenization step in liquid culture was conducted without any antibiotic selection (see Materials and Methods). Our assays, which were conducted under laboratory conditions, may or may not be the most optimal for lysogenization, since transduction under "in vivo" conditions seems to be very effective (25,26,28,29). The Stx phage induced from the Norwegian O103:H25 isolate was shown to be capable of lysogeny after storage in a dry-fermented sausage model (36).…”

Section: Discussionmentioning

confidence: 99%

“…However, the transduction of stx genes could lead to the emergence of new pathogenic clones that have not yet been described. Among multiple examples of bacterial conversion by Stx phages in vivo and in vitro (16,(25)(26)(27)(28)(29), the STEC O104:H4 strain that caused the huge outbreak of HUS in Germany in May 2011, and that also affected France, is the most recent case (30,31). The German O104:H4 strain presumably acquired the Stx phage in a late evolutionary event, generating a highly virulent pathogen that, unlike other enteroaggregative E. coli strains, produced the Shiga toxin (32).…”

Section: Discussionmentioning

confidence: 99%

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Persistence of Infectious Shiga Toxin-Encoding Bacteriophages after Disinfection Treatments

Allué-Guardia

Martínez-Castillo

Muniesa

2014

Appl Environ Microbiol

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In Shiga toxin-producing Escherichia coli (STEC), induction of Shiga toxin-encoding bacteriophages (Stx phages) causes the release of free phages that can later be found in the environment. The ability of Stx phages to survive different inactivation conditions determines their prevalence in the environment, the risk of stx transduction, and the generation of new STEC strains. We evaluated the infectivity and genomes of two Stx phages (⌽534 and ⌽557) under different conditions. Infectious Stx phages were stable at 4, 22, and 37°C and at pH 7 and 9 after 1 month of storage but were completely inactivated at pH 3. Infective Stx phages decreased moderately when treated with UV (2.2-log 10 reduction for an estimated UV dose of 178.2 mJ/cm 2 ) or after treatment at 60 and 68°C for 60 min (2.2-and 2.5-log 10 reductions, respectively) and were highly inactivated (3 log 10 ) by 10 ppm of chlorine in 1 min. Assays in a mesocosm showed lower inactivation of all microorganisms in winter than in summer. The number of Stx phage genomes did not decrease significantly in most cases, and STEC inactivation was higher than phage inactivation under all conditions. Moreover, Stx phages retained the ability to lysogenize E. coli after some of the treatments. Shiga toxin-producing Escherichia coli (STEC) strains are pathogenic and cause a wide range of diseases, with symptoms varying from noncomplicated diarrhea to the life-threatening hemolytic-uremic syndrome (HUS) (1, 2). STEC produces two immunologically distinct toxins known as Shiga toxin 1 (Stx1) and Shiga toxin 2 (Stx2), and both toxins present diverse variants (1).The genes encoding Stx in E. coli are located in the genomes of inducible temperate bacteriophages (Stx phages) (3). Induction of the lytic cycle of Stx phages causes an increase in production of Shiga toxin, which is the virulence factor responsible for severe complications associated with the infection, such as HUS (2, 4). In addition to the increase in Stx expression, the lysis of the cell caused by Stx phages allows the release of Stx outside the cell and also the dissemination of Stx phages. Free Stx phages spread within the gut and are excreted with the feces (5). In terms of occurrence in the environment, Stx phages have been found in water bodies containing fecal contamination of human or animal origin (6-12). Infectious Stx phages have also been detected in food samples, and despite the abundance of Stx phages in these samples, they showed levels of bacterial indicators (aerobic colony counts and E. coli) that make them acceptable for consumption according to European regulations (13).The widespread distribution of Stx phages in different environments indicates that they must be able to persist under diverse conditions. Previous studies suggested the persistence of environmental Stx phages (7). Newly developed molecular methods for the quantification of Stx phages (14), the development of new approaches for the optimal detection of plaques formed by infectious Stx phages (15), and optimized protocols for th...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Persistence of Infectious Shiga Toxin-Encoding Bacteriophages after Disinfection Treatments

Allué-Guardia

Martínez-Castillo

Muniesa

2014

Appl Environ Microbiol

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“…The Stx2-encoding bacteriophage ⌽731 (⌬stx 2 ::cat) (hereinafter called ⌽731) was inserted into the chromosome of E. coli isolates and confirmed to be stable and functioning, as described previously (20). The original bacteriophage was carried by an E. coli O103:H25 strain from a Norwegian HUS patient (25).…”

Section: Methodsmentioning

confidence: 99%

“…A correlation between biofilm-forming abilities and persistence in food and feed-producing facilities has been reported for Salmonella enterica (18) and Listeria monocytogenes (19), and it has been suggested that biofilms in food-producing environments may serve as reservoirs for bacteria that may contaminate the food products. Furthermore, we have previously shown that dissemination of virulence genes like stx can occur in E. coli biofilm (20). Consequently, biofilms can also be environments for the evolution of new pathogenic E. coli isolates.…”

mentioning

confidence: 99%

Potentially Pathogenic Escherichia coli Can Form a Biofilm under Conditions Relevant to the Food Production Chain

Nesse

Sekse

Berg

et al. 2014

Appl Environ Microbiol

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The biofilm-producing abilities of potentially human-pathogenic serotypes of Escherichia coli from the ovine reservoir were studied at different temperatures and on different surfaces. A possible influence of the hydrophobicity of the bacterial cells, as well as the presence of two virulence factors, the Shiga toxin-encoding (Stx) bacteriophage and the eae gene, was also studied. A total of 99 E. coli isolates of serotypes O26:H11, O103:H2, and O103:H25 isolated from sheep feces were included. The results show that isolates of all three E. coli serotypes investigated can produce biofilm on stainless steel, glass, and polystyrene at 12, 20, and 37°C. There was a good general correlation between the results obtained on the different surfaces. E. coli O103:H2 isolates produced much more biofilm than those of the other two serotypes at all three temperatures. In addition, isolates of serotype O26:H11 produced more biofilm than those of O103:H25 at 37°C. The hydrophobicity of the isolates varied between serotypes and was also influenced by temperature. The results strongly indicated that hydrophobicity influenced the attachment of the bacteria rather than their ability to form biofilm once attached. Isolates with the eae gene produced less biofilm at 37°C than isolates without this gene. The presence of a Stx bacteriophage did not influence biofilm production. In conclusion, our results show that potentially human-pathogenic E. coli from the ovine reservoir can form biofilm on various surfaces and at several temperatures relevant for food production and handling.

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“…Some studies have shown that transmission of stx phages may occur in water (Imamovic et al, 2009), in various food matrices (e.g. milk, orange juice, salad and ground beef) (Imamovic et al, 2009;Picozzi et al, 2012) and also in biofilms (Solheim et al, 2013).…”

Section: Dissemination Of Stx Phages Outside the Intestinementioning

confidence: 99%

Shiga toxins and stx phages: highly diverse entities

2015

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Shiga toxins are the main virulence factors of a group of Escherichia coli strains [Shiga toxinproducing E. coli (STEC)] that cause severe human diseases, such as haemorrhagic colitis and haemolytic-uraemic syndrome. The Shiga toxin family comprises several toxin subtypes, which have been differentially related to clinical manifestations. In addition, the phages that carry the Shiga toxin genes (stx phages) are also diverse. These phages play an important role not only in the dissemination of Shiga toxin genes and the emergence of new STEC strains, but also in the regulation of Shiga toxin production. Consequently, differences in stx phages may affect the dissemination of stx genes as well as the virulence of STEC strains. In addition to presenting an overview of Shiga toxins and stx phages, in this review we highlight current knowledge about the diversity of stx phages, with emphasis on its impact on STEC virulence. We consider that this diversity should be taken into account when developing STEC infection treatments and diagnostic approaches, and when conducting STEC control in reservoirs.

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Biofilm as an Environment for Dissemination of stx Genes by Transduction

Cited by 47 publications

References 27 publications

Persistence of Infectious Shiga Toxin-Encoding Bacteriophages after Disinfection Treatments

Persistence of Infectious Shiga Toxin-Encoding Bacteriophages after Disinfection Treatments

Potentially Pathogenic Escherichia coli Can Form a Biofilm under Conditions Relevant to the Food Production Chain

Shiga toxins and stx phages: highly diverse entities

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