Monitoring Urban Beach Quality on a Summer Day: Determination of the Origin of Fecal Indicator Bacteria and Antimicrobial Resistance at Prophète Beach, Marseille (France)

Abstract

A highly frequented beach in Marseille, France, was monitored on an hourly basis during a summer day in July 2018, to determine possible water and sand fecal pollution, in parallel with influx of beach users from 8 a.m. to 8 p.m. Fecal indicator bacteria were enumerated, together with four host-associated fecal molecular markers selected to discriminate human, dog, horse, or gull/seagull origins of the contamination. The antimicrobial resistance of bacteria in water and sand was evaluated by quantifying (i) the class 1, 2, and 3 integron integrase genes intI, and (ii) blaTEM, blaCTX–M, and blaSHV genes encoding endemic beta-lactamase enzymes. The number of beach users entering and leaving per hour during the observation period was manually counted. Photographs of the beach and the bathing area were taken every hour and used to count the number of persons in the water and on the sand, using a photo-interpretation method. The number of beach users increased from early morning to a peak by mid-afternoon, totaling more than 1,800, a very large number of users for such a small beach (less than 1 ha). An increase in fecal contamination in the water corresponded to the increase in beach attendance and number of bathers, with maximum numbers observed in the mid-afternoon. The human-specific fecal molecular marker HF183 indicated the contamination was of human origin. In the water, the load of Intl2 and 3 genes was lower than Intl1 but these genes were detected only during peak attendance and highest fecal contamination. The dynamics of the genes encoding B-lactamases involved in B-lactams resistance notably was linked to beach attendance and human fecal contamination. Fecal indicator bacteria, integron integrase genes intI, and genes encoding B-lactamases were detected in the sand. This study shows that bathers and beach users can be significant contributors to contamination of seawater and beach sand with bacteria of fecal origin and with bacteria carrying integron-integrase genes and beta lactamase encoding genes. High influx of users to beaches is a significant factor to be considered in order to reduce contamination and manage public health risk.

Characterization of the Pathogenic Potential of the Beach Sand Microbiome and Assessment of Quicklime as a Remediation Tool

“…Limitations of the study include the period during which the analyses were performed (November–June), since the microbial contamination of human origin is expected to increase significantly during the summer season, due to the increased presence of people on the beaches [ 43 ]. Thus, the study should be extended to summer period to get generalizable results.…”

Genetic sequence data evidence that human faecal-associated HF183 sequences are on human skin and in urine

“…HF183 has been consistently detected in beach waters along California coast (Cao et al, 2017; McQuaig et al, 2012; Russell et al, 2013; Sercu et al, 2009), and public health risks have been estimated based on quantitative microbial risk assessment (QMRA) of HF183 detection levels (Boehm et al, 2015; Brown et al, 2017). Correlations between swimmers and the presence of low levels of HF183 have been reported, suggesting bather shedding as a source of HF183 to recreational waters (Li, Van De Werfhorst, Steets, Ervin, Murray, Blackwell, et al, 2021; Li, van De Werfhorst, Steets, Ervin, Murray, Devarajan, & Holden, 2021; Toubiana et al, 2021). The results of this study may inform such correlations by suggesting that B. dorei in skin or urine microbiomes of bathers might contribute to the observed low levels of HF183 in environmental waters.…”

“…HF183 was also consistently observed in beach waters along the California coast in many previous studies associated with sampled drainage, creek and river waters (Cao et al, 2017; McQuaig et al, 2012; Russell et al, 2013; Sercu et al, 2009). In recent studies of several beaches, swimmers were found to be sources of chronic, low concentration, HF183 markers in beach surf zone waters (Li, Van De Werfhorst, Steets, Ervin, Murray, Blackwell, et al, 2021; Li, van De Werfhorst, Steets, Ervin, Murray, Devarajan, & Holden, 2021; Toubiana et al, 2021). These results raised the question: could aquatic HF183 detections originate from other than human faecal releases or faecal shedding into the environment?…”

“…In the last decade, numerous studies have been performed to reveal human skin and urine microbiomes (Fouts et al, 2012; Grice et al, 2009; Lehtimäki et al, 2017; Lewis et al, 2013; Meisel et al, 2016; Oh et al, 2014; Siddiqui et al, 2011; Turnbaugh et al, 2007; van Rensburg et al, 2015). Considering the possibilities for contamination of human body skin and the urinary tract by HF183 and human‐associated B. dorei , as well as the potential for any HF183 populations on humans to be sources to environmental waters during bather shedding (Li, Van De Werfhorst, Steets, Ervin, Murray, Blackwell, et al, 2021; Li, van De Werfhorst, Steets, Ervin, Murray, Devarajan, & Holden, 2021; Toubiana et al, 2021), it is worth determining whether HF183 and human‐associated B. dorei are within sequences associated with human skin and urine microbiomes. In this study, we examine this issue based on secondary examination of previously published human skin and urine microbiome gene sequence data.…”

An Overview of Microbial Source Tracking Using Host-Specific Genetic Markers to Identify Origins of Fecal Contamination in Different Water Environments

“…A considerable number of studies have focused on recreational beach waters, which are greatly associated with human activities and public health. Humans/sewage inputs have been frequently identified as the major pollution sources on public urban beaches [92], urban runoff-impacted beaches [93], marine beaches [94], coastal beaches [95], and surfing beaches [96], often using HF183 and HumM2 MST markers. Bathers and beach users/visitors were considered to contribute directly and significantly to the resulting fecal pollution, which is exacerbated by stormwater discharge.…”