Spatial and temporal variation in indicator microbe sampling is influential in beach management decisions

Enns, Amber A.; Vogel, Laura J.; Abdelzaher, Amir M.; Solo‐Gabriele, Helena M.; Plano, Lisa R. W.; Gidley, Maribeth L.; Phillips, Matthew C.; Klaus, James S.; Piggot, Alan M.; Feng, Zhixuan; Reniers, Ad; Haus, Brian K.; Elmir, Samir M.; Zhang, Yifan; Jimenez, Nasly H.; Abdel-Mottaleb, Noha; Schoor, Michael E.; Alexis, Brown; Khan, S.; Dameron, Adrienne S.; Salazar, Norma C.; Fleming, Lora E.

doi:10.1016/j.watres.2012.01.040

Cited by 69 publications

(54 citation statements)

References 30 publications

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“…We found that community changes correlated with nutrient concentrations in berm sand. Nutrients are relatively more conserved than E. coli and enterococci, which can die off in short periods of time and be highly transient (50,(54)(55)(56)(57). These findings support that nutrient concentrations and microbial communities are relatively stable over time and reflect longer-term conditions at a beach better than densities of fecal indicators.…”

Section: Discussionmentioning

confidence: 52%

Influence of Land Use, Nutrients, and Geography on Microbial Communities and Fecal Indicator Abundance at Lake Michigan Beaches

Cloutier

Alm

McLellan

2015

Appl Environ Microbiol

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bMicrobial communities within beach sand play a key role in nutrient cycling and are important to the nearshore ecosystem function. Escherichia coli and enterococci, two common indicators of fecal pollution, have been shown to persist in the beach sand, but little is known about how microbial community assemblages are related to these fecal indicator bacteria (FIB) reservoirs. We examined eight beaches across a geographic gradient and range of land use types and characterized the indigenous community structure in the water and the backshore, berm, and submerged sands. FIB were found at similar levels in sand at beaches adjacent to urban, forested, and agricultural land and in both the berm and backshore. However, there were striking differences in the berm and backshore microbial communities, even within the same beach, reflecting the very different environmental conditions in these beach zones in which FIB can survive. In contrast, the microbial communities in a particular beach zone were similar among beaches, including at beaches on opposite shores of Lake Michigan. The differences in the microbial communities that did exist within a beach zone correlated to nutrient levels, which varied among geographic locations. Total organic carbon and total phosphorus were higher in Wisconsin beach sand than in beach sand from Michigan. Within predominate genera, finescale sequence differences could be found that distinguished the populations from the two states, suggesting a biogeographic effect. This work demonstrates that microbial communities are reflective of environmental conditions at freshwater beaches and are able to provide useful information regarding long-term anthropogenic stress. Since the creation of the Federal Beach Environmental Assessment and Coastal Health (BEACH) Act of 2000, coastal communities have been challenged with implementing programs for the monitoring of recreational waters. Water quality monitoring relies on fecal indicator bacteria (FIB), such as Escherichia coli and enterococci, and the assumption that both are fecal in origin. In recent years, many Great Lakes coastal recreational waters were monitored for the first time and subsequently were found to have unacceptable levels of E. coli, indicating the presence of contamination from sources such as sewage, stormwater, or agricultural runoff. However, recent studies have detected high concentrations of FIB in recreational beach sands compared to the concentrations in the nearby monitored waters (1-4). Importantly, several studies have documented that sand reservoirs of FIB play a large role in beach water samples exceeding regulatory limits (1, 3, 5-7).Persistent FIB in the beach environment is of great concern. The presence of FIB in either recreational waters or sand is assumed to indicate a recent pollution event. However, the persistence and possible proliferation of FIB in the beach environment can confound beach-monitoring efforts and poses additional challenges for beach managers. In addition, there is mounting evidence that E. co...

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Section: Discussionmentioning

confidence: 52%

Influence of Land Use, Nutrients, and Geography on Microbial Communities and Fecal Indicator Abundance at Lake Michigan Beaches

Cloutier

Alm

McLellan

2015

Appl Environ Microbiol

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“…The concentrations of these bacteria, however, are known to be highly variable (6,7,59,60). Intensive field studies show that their concentrations fluctuate on diurnal timescales due to sunlight exposure; concentrations drop during sunlit hours and rise after the sun sets (8,21,50,60,61). While enterococcal photoinactivation is well documented, the mechanisms of inactivation are not well understood, limiting our ability to predict when the process will be important under the wide range of conditions that exist in natural and engineered systems.…”

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confidence: 99%

Mechanisms for Photoinactivation of Enterococcus faecalis in Seawater

Sassoubre

Nelson

Boehm

2012

Appl Environ Microbiol

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bField studies in fresh and marine waters consistently show diel fluctuations in concentrations of enterococci, indicators of water quality. We investigated sunlight inactivation of Enterococcus faecalis to gain insight into photoinactivation mechanisms and cellular responses to photostress. E. faecalis bacteria were exposed to natural sunlight in clear, filtered seawater under both oxic and anoxic conditions to test the relative importance of oxygen-mediated and non-oxygen-mediated photoinactivation mechanisms. Multiple methods were used to assess changes in bacterial concentration, including cultivation, quantitative PCR (qPCR), propidium monoazide (PMA)-qPCR, LIVE/DEAD staining using propidium iodide (PI), and cellular activity, including ATP concentrations and expression of the superoxide dismutase-encoding gene, sodA. Photoinactivation, based on numbers of cultivable cells, was faster in oxic than in anoxic microcosms exposed to sunlight, suggesting that oxygen-mediated photoinactivation dominated. There was little change in qPCR signal over the course of the experiment, demonstrating that the nucleic acid targets were not damaged to a significant extent. The PMA-qPCR signal was also fairly stable, consistent with the observation that the fraction of PI-permeable cells was constant. Thus, damage to the membrane was minimal. Microbial ATP concentrations decreased in all microcosms, particularly the sunlit oxic microcosms. The increase in relative expression of the sodA gene in the sunlit oxic microcosms suggests that cells were actively responding to oxidative stress. Dark repair was not observed. This research furthers our understanding of photoinactivation mechanisms and the conditions under which diel fluctuations in enterococci can be expected in natural and engineered systems. H ealth risks posed by exposure to polluted recreational waters are assessed using levels of the fecal indicator bacteria Enterococcus spp. and Escherichia coli. The concentrations of these bacteria, however, are known to be highly variable (6,7,59,60). Intensive field studies show that their concentrations fluctuate on diurnal timescales due to sunlight exposure; concentrations drop during sunlit hours and rise after the sun sets (8,21,50,60,61). While enterococcal photoinactivation is well documented, the mechanisms of inactivation are not well understood, limiting our ability to predict when the process will be important under the wide range of conditions that exist in natural and engineered systems.Bacterial photoinactivation is the result of direct and indirect damage caused by sunlight exposure. Direct damage occurs when photons are absorbed directly by cellular molecules, leading to changes in chemical bond structure. The most common example is UVB damage to DNA, resulting in pyrimidine dimers that prevent DNA replication (39, 47, 51). Indirect damage can occur when photons are absorbed by endogenous (intracellular) sensitizers, such as porphyrins and flavins, or exogenous (extracellular) sensitizers, such as humic compound...

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“…Hourly sampling in South Korea resulted in similar conclusions: under dry weather conditions, sunlight inactivation of enterococci was responsible for a reduction of 1 to 2 orders of magnitude (59). A recent study showed that exceedances of current regulatory standards for enterococci at marine beaches (i.e., 104 CFU/100 ml) are more frequent during the night and late-afternoon hours (from approximately 6 p.m. to 8 a.m.) than during the morning and early afternoon, suggesting that sampling at different times of the day can significantly influence beach management decisions (100). Interestingly, a recent study described a possible mechanism for the extended survival of some enterococcal species exposed to sunlight: carotenoid pigment quenching of reactive oxygen species in certain strains appears to confer a competitive advantage against sunlight-induced inactivation (over nonpigmented isolates) (217).…”

Section: Responses To Environmental Stressorsmentioning

confidence: 99%

Enterococci in the Environment

Byappanahalli

Nevers

Korajkic

et al. 2012

Microbiol Mol Biol Rev

564

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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Spatial and temporal variation in indicator microbe sampling is influential in beach management decisions

Cited by 69 publications

References 30 publications

Influence of Land Use, Nutrients, and Geography on Microbial Communities and Fecal Indicator Abundance at Lake Michigan Beaches

Influence of Land Use, Nutrients, and Geography on Microbial Communities and Fecal Indicator Abundance at Lake Michigan Beaches

Mechanisms for Photoinactivation of Enterococcus faecalis in Seawater

Enterococci in the Environment

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