Analysis of the Gull Fecal Microbial Community Reveals the Dominance of Catellicoccus marimammalium in Relation to Culturable Enterococci

2017

Appl Environ Microbiol

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Alternative indicators have been developed that can be used to identify host sources of fecal pollution, yet little is known about how their distribution and fate compare to traditional indicators. Escherichia coli and enterococci were widely distributed at the six beaches studied and were detected in almost 95% of water samples (n ϭ 422) and 100% of sand samples (n ϭ 400). Berm sand contained the largest amount of E. coli (P Ͻ 0.01), whereas levels of enterococci were highest in the backshore (P Ͻ 0.01). E. coli and enterococci were the lowest in water, using a weight-to-volume comparison. The gull-associated Catellicoccus marimammalium (Gull2) marker was found in over 80% of water samples, regardless of E. coli levels, and in 25% of sand samples. Human-associated Bacteroides (HB) and Lachnospiraceae (Lachno2) were detected in only 2.4% of water samples collected under baseflow and post-rain conditions but produced a robust signal after a combined sewage overflow, despite low E. coli concentrations. Burdens of E. coli and enterococci in water and sand were disproportionately high in relation to alternative indicators when comparing environmental samples to source material. In microcosm studies, Gull2, HB, and Lachno2 quantitative PCR (qPCR) signals were reduced twice as quickly as those from E. coli and enterococci and approximately 20% faster than signals from culturable E. coli. High concentrations of alternative indicators in source material illustrated their high sensitivity for the identification of fecal sources; however, differential survival and the potential for long-term persistence of traditional fecal indicators complicate the use of alternative indicator data to account for the levels of E. coli and enterococci in environmental samples. IMPORTANCE E. coli and enterococci are general indicators of fecal pollution and may persist in beach sand, making their use problematic for many applications. This study demonstrates that gull fecal pollution is widespread at Great Lakes beaches, whereas human and ruminant contamination is evident only after major rain events. An exploration of sand as a reservoir for indicators found that E. coli was ubiquitous, while gull host markers were detected in only 25% of samples. In situ sand beach microcosms provided decay rate constants for E. coli and enterococci relative to alternative indicators, which establish comparative benchmarks that would be helpful to distinguish recent from past pollution. Overall, alternative indicators are useful for identifying sources and assessing potentially high health risk contamination events; however, beach managers should be cautious in attempting to directly link their detection to the levels of E. coli or enterococci.KEYWORDS beaches, water quality, human-associated indicators, gull-associated indicators, qPCR F ecal contamination of recreational waters can be a serious threat to public health. Due to the vast diversity of fecal-borne human pathogens, the USEPA has recommended the use of fecal indicator bacteria (FIB),...

Section: Discussionmentioning

confidence: 52%

Distribution and Differential Survival of Traditional and Alternative Indicators of Fecal Pollution at Freshwater Beaches

Cloutier

2017

Appl Environ Microbiol

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“…Gulls, other shorebirds and waterfowl are suspect fecal pollution sources at many beaches. Gulls appear to harbor very different fecal microbial communities than humans, one that is dominated by enterococci and E. coli , with a limited number of fecal anaerobes [27, 112, 113]. Based on cloning of the microbial community, a genetic marker targeting Catellicoccus marimammalium was described by Lu and colleagues [112].…”

Section: Concluding Remarks and Future Directionsmentioning

confidence: 99%

“…Based on cloning of the microbial community, a genetic marker targeting Catellicoccus marimammalium was described by Lu and colleagues [112]. Deep sequencing demonstrated this organism was the dominant community member (in some cases comprising >90% of the total community) in gull feces and much more abundant then traditional enterococci fecal indicators [113]. Comparison with sewage samples that were also deeply sequenced [100] suggested this target was completely absent in sewage and therefore potentially a reliable marker to complement sewage indictors at beaches.…”

Section: Concluding Remarks and Future Directionsmentioning

confidence: 99%

Discovering new indicators of fecal pollution

Eren

2014

Trends in Microbiology

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149

106

Fecal pollution indicators are essential to identify and remediate contamination sources and protect public health. Historically, easily cultured facultative anaerobes such as fecal coliforms, Escherichia coli, or enterococci have been used, but these indicators generally provide no information as to their source. More recently, molecular methods have targeted fecal anaerobes, which are much more abundant in humans and other mammals and some strains appear to be associated with certain host sources. Next-generation sequencing and microbiome studies have created an unprecedented inventory of microbial communities associated with fecal sources, allowing reexamination of which taxonomic groups are best suited as informative indicators. The use of new computational methods, such as oligotyping coupled with well-established machine learning approaches, is providing new insights into patterns of host association. In this review we examine the basis for host-specificity and the rationale for using 16S rRNA gene targets for alternative indicators and highlight two taxonomic groups, Bacteroidales and Lachnospiraceae, which are rich in host-specific bacterial organisms. Finally, we discuss considerations for using alternative indicators for water quality assessments with a particular focus on detecting human sewage sources of contamination.

“…To assess the levels of E. coli and enterococcus reads in our community sequences, we used the SRA BLAST tool. We performed a BLAST of the community sequences from the present study (SRP052297) against 16S sequences of enterococci (accession numbers KF250762 to KF250872) (34) and E. coli (X80724) obtained from GenBank.…”

Section: Methodsmentioning

confidence: 99%

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

Cloutier

Alm

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...