Characterization of Enterococcus faecalis-infecting phages (enterophages) as markers of human fecal pollution in recreational waters

Santiago-Rodríguez, Tasha M.; Dávila, Catalina; González, Joel Pérez; Bonilla, Natasha; Marcos, Patricia; Urdaneta, Miguel; Cadete, M.; Monteiro, Sílvia; Santos, Ricardo; Domingo, Jorge Santo; Toranzos, Gary A.

doi:10.1016/j.watres.2010.07.078

Cited by 30 publications

(37 citation statements)

References 41 publications

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“…Bacteriophages that infect various Enterococcus spp. ("enterophage") from different sources (i.e., raw sewage, cow manure, and environmental waters) were recently described (31,223,268,279). However, the effect of enterophage on bacterial survival was not tested directly, since the main objective of these works was to examine the utility of enterophage as a microbial source tracking marker.…”

Section: Responses To Environmental Stressorsmentioning

confidence: 99%

Enterococci in the Environment

Byappanahalli

Nevers

Korajkic

et al. 2012

Microbiol Mol Biol Rev

565

383

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SUMMARYEnterococci are common, commensal members of gut communities in mammals and birds, yet they are also opportunistic pathogens that cause millions of human and animal infections annually. Because they are shed in human and animal feces, are readily culturable, and predict human health risks from exposure to polluted recreational waters, they are used as surrogates for waterborne pathogens and as fecal indicator bacteria (FIB) in research and in water quality testing throughout the world. Evidence from several decades of research demonstrates, however, that enterococci may be present in high densities in the absence of obvious fecal sources and that environmental reservoirs of these FIB are important sources and sinks, with the potential to impact water quality. This review focuses on the distribution and microbial ecology of enterococci in environmental (secondary) habitats, including the effect of environmental stressors; an outline of their known and apparent sources, sinks, and fluxes; and an overview of the use of enterococci as FIB. Finally, the significance of emerging methodologies, such as microbial source tracking (MST) and empirical predictive models, as tools in water quality monitoring is addressed. The mounting evidence for widespread extraenteric sources and reservoirs of enterococci demonstrates the versatility of the genusEnterococcusand argues for the necessity of a better understanding of their ecology in natural environments, as well as their roles as opportunistic pathogens and indicators of human pathogens.

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Section: Responses To Environmental Stressorsmentioning

confidence: 99%

Enterococci in the Environment

Byappanahalli

Nevers

Korajkic

et al. 2012

Microbiol Mol Biol Rev

565

383

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“…Experiments were performed during a period of low and higher rainfall events and included: (i) the highest and thus one of the less polluted sites of the watershed (site 1), (ii) immediately after a WTP (site 2), since it represents a point-source of fecal contamination, and (iii) the estuary (site 3). The survival experiments were conducted as described above and seeded samples were kept at 22 °C, the average temperature of waters in Puerto Rico (Santiago-Rodriguez et al 2010). All precipitation data were obtained from the US Geological Survey (USGS) Caribbean Water Science Center, stations 50020100, 50024950, and 50021700 (http://pr.water.usgs.…”

Section: Inactivation Rates and Survival Studiesmentioning

confidence: 99%

“…For this reason, we have proposed phages that infect a specific type strain of Enterococcus faecalis (enterophages) as markers of human fecal contamination. Most enterophage isolates characterized in our laboratory are tailed phages, with icosahedral capsids measuring between 13 and 80 nm and DNA genomes >23 kbp Santiago-Rodriguez et al 2010). In terms of their reliability as indicators of human fecal pollution, enterophages: (i) have been detected in raw and treated domestic sewage Santiago-Rodriguez et al 2010), (ii) possess a survival similar to that of many enteric viruses in fresh waters (Rao et al 1984;Ward et al 1986), and (iii) have not been detected in cattle feces.…”

Section: Introductionmentioning

confidence: 99%

“…Most enterophage isolates characterized in our laboratory are tailed phages, with icosahedral capsids measuring between 13 and 80 nm and DNA genomes >23 kbp Santiago-Rodriguez et al 2010). In terms of their reliability as indicators of human fecal pollution, enterophages: (i) have been detected in raw and treated domestic sewage Santiago-Rodriguez et al 2010), (ii) possess a survival similar to that of many enteric viruses in fresh waters (Rao et al 1984;Ward et al 1986), and (iii) have not been detected in cattle feces. Even though previous results have been promising, more data are needed to fully determine the potential of enterophages as indicators of human fecal contamination.…”

Section: Introductionmentioning

confidence: 99%

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Evaluation of Enterococcus-infecting phages as indices of fecal pollution

Santiago-Rodríguez

Marcos

Monteiro

et al. 2012

Journal of Water and Health

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No microbial source tracking tool satisfies all the characteristics of an ideal indicator of human fecal pollution. For this reason, the potential of Enterococcus faecalis phages (enterophages) as markers of this type of contamination was tested by using eight Enterococcus type strains as the possible hosts. The prevalence of enterophages in animal feces and domestic sewage were determined, as were the inactivation rates in raw sewage at 4 °C and surface and tap waters at 22 °C. Enterophages were exclusively detected in raw sewage (up to 66.0 plaque forming units (PFU)/100 mL), suggesting a strictly human origin; and exhibited inactivation rates of approximately 0.002 to 0.05, 0.3 to 0.5 and 0.4 to 1.4 log day(-1) in raw sewage and surface and tap waters, respectively, similar to those of previous reports on human enteric viruses under similar conditions. Interestingly, phages infecting other Enterococcus type strains were detected in both animal feces and domestic sewage in concentrations of up to 335.8 PFU/g and 96.0 PFU/100 mL, and certain phage isolates infected several of the strains tested. This clearly indicates the possible promiscuous nature of some Enterococcus phages and thus opens up the opportunity to further characterize these as indices of specific fecal sources.

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“…Enterophages have a survival time similar to that of human enteric viruses in marine and fresh waters and sand (8,32,36,43), have been detected in raw and treated domestic sewage in Puerto Rico and Portugal, and have been detected neither in pristine waters nor in animal feces (e.g., pigs, dogs, cattle, and chickens) (8,36). However, more data are needed in order to accept enterophages as alternate indicators of human fecal contamination.…”

mentioning

confidence: 99%

Microbial Quality of Tropical Inland Waters and Effects of Rainfall Events

Santiago-Rodríguez

Tremblay

Toledo-Hernández

et al. 2012

Appl Environ Microbiol

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dNovel markers of fecal pollution in tropical waters are needed since conventional methods recommended for other geographical regions may not apply. To address this, the prevalence of thermotolerant coliforms, enterococci, coliphages, and enterophages was determined by culture methods across a watershed. Additionally, human-, chicken-, and cattle-specific PCR assays were used to identify potential fecal pollution sources in this watershed. An enterococcus quantitative PCR (qPCR) assay was tested and correlated with culture methods at three sites since water quality guidelines could incorporate this technique as a rapid detection method. Various rainfall events reported before sample collection at three sites were considered in the data analyses. Thermotolerant coliforms, enterococci, coliphages, and enterophages were detected across the watershed. Human-specific Bacteroides bacteria, unlike the cattle-and chicken-specific bacteria, were detected mostly at sites with the corresponding fecal impact. Enterococci were detected by qPCR as well, but positive correlations with the culture method were noted at two sites, suggesting that either technique could be used. However, no positive correlations were noted for an inland lake tested, suggesting that qPCR may not be suitable for all water bodies. Concentrations of thermotolerant coliforms and bacteriophages were consistently lower after rainfall events, pointing to a possible dilution effect. Rainfall positively correlated with enterococci detected by culturing and qPCR, but this was not the case for the inland lake. The toolbox of methods and correlations presented here could be potentially applied to assess the microbial quality of various water types.

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Characterization of Enterococcus faecalis-infecting phages (enterophages) as markers of human fecal pollution in recreational waters

Cited by 30 publications

References 41 publications

Enterococci in the Environment

Enterococci in the Environment

Evaluation of Enterococcus-infecting phages as indices of fecal pollution

Microbial Quality of Tropical Inland Waters and Effects of Rainfall Events

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