Methicillin-resistant Staphylococcus aureus in Southern California coastal waters: environmental exposure to humans and stormwater biofilters as a preventative solution
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Methicillin-resistant Staphylococcus aureus in Southern California coastal waters: environmental exposure to humans and stormwater biofilters as a preventative solution


Antibiotic resistance is one of the greatest challenges to modern global health. Sources of antibiotic resistant bacteria (ARB) and antibiotic resistances genes (ARGs) to surface water include wastewater treatment plants, medical waste streams, and agricultural sites. Recent studies have identified stormwater as a source of ARGs, and often stormwater contains other contaminants such as heavy metals and antibiotics that select for antibiotic resistance. As an emerging contaminant, ARB and ARGs are not regulated or traditionally monitored in recreational swimming waters that may receive stormwater runoff. This research is divided into two parts: 1) Chapter 1 is an epidemiological study on surfers’ exposure to ARB in the ocean, and 2) Chapters 2 and 3 investigate the fate and transport of ARB, ARGs, and other pathogens and indicators in stormwater biofilters.Exposure to sources of ARB has been associated with colonization and infection in human populations, and recent work suggests the environment serves as an open reservoir available for transferring human pathogens. Surfers are a unique population for evaluating the relationship between environmental exposure and ARB colonization. Surfing involves a high frequency of unanticipated head submersions, exposures of long duration, and surfers are in the ocean year-round, particularly in the winter when storms occur, resulting in poor water quality due to urban stormwater contaminants. Beginning Fall 2018, two Santa Monica Bay surfing beaches were monitored for Methicillin-resistant Staphylococcus aureus (MRSA). Nasal swab samples were concurrently taken from a group of surfers and a non-surfing control group to investigate how this pathogen colonizes humans. Presumptive MRSA was always detected in marine samples, with highly elevated levels observed after stormwater runoff events. Surfers that surfed during wet-weather events were over six times more likely to be colonized by MRSA compared to controls, and also over three times more likely to be colonized than dry-weather surfers. This research suggests that the ocean may be an important reservoir of MRSA and have a special role in pathogen transmission to humans. Stormwater biofilters are a promising passive treatment solution for reducing microbial pollution in surface waters. While bioretention systems (biofilters) have been widely and effectively used to capture chemical pollutants from surface runoff, the effect of biofilters on both heavy metals and antibiotic resistance genes (ARGs) has been relatively understudied. The co-occurrence of heavy metals and ARGs is important because of known heavy metal co-selection in environmental compartments. Surface soil samples from six biofilters and bioswales in Southern California over three time periods were analyzed for ARGs, mobile genetic element (intI1), and 16S rRNA (proxy for total bacterial load). The impact of soil properties and the co-selective effect of nine heavy metals (both bioavailable fraction and total) on ARG levels in the biofilters were also investigated. Both relative sul1 and intI1 levels in biofilters were statistically greater than those detected in pristine soils. Total concentrations of arsenic, copper, lead, vanadium, and zinc exhibited significant correlations individually with relative abundances of sul1, sul2, tetW, and intI1. Soil organic matter, total nitrogen, total carbon, and the percentage of sand and silt within biofilters appeared to be significantly associated with absolute gene abundances of sul1, sul2, and tetW. Stronger relationships were found using a multiple linear regression model, suggesting multiple effects of soil properties, in addition to bioavailable and total heavy metals on the microorganisms within biofilters. While stormwater biofilters have been shown to remove chemical contaminants such as nutrients and heavy metals, their efficacy in removing microbial pathogens has been understudied. Full-scale biofilter studies are rare as most biofilter research has been conducted with laboratory-scale biofilters. Additionally, microbial removal is typically evaluated using traditional fecal indicator bacteria (FIB) as a proxy for pathogen removal, and it is not known if traditional indicators accurately reflect pathogen removal within biofilters. A pilot-scale biofilter located on the Glassell Public Works campus (Orange, CA) was synergistically studied for removal of conventional fecal indicators, bacterial and viral fecal source markers, antibiotic resistance genes, and bacterial and viral pathogens. Log reduction of fecal indicator bacteria (both genetic and culture-based) was high. Some of the pathogens tested were effectively removed, while the biofilter itself served as a reservoir for two pathogens (Campylobacter and Salmonella). The removal of HF183 did not match FIB or pathogen removal, with no removal observed. Viral fecal source markers PMMoV and crAssphage had satisfactory log reductions that were more comparable to those observed in both FIB and some pathogens. ARGs and intI1 showed gene-specific log reduction. These findings suggest that FIB and fecal source markers may not adequately represent pathogen removal in stormwater biofilters. This research will enhance our knowledge of the fate and transport of ARG and ARB in surface water and stormwater biofilter infrastructure. Additionally, it will serve to further our understanding of how the environment may transfer ARB to humans. The results of this research can illuminate appropriate public health responses and mitigation efforts for reducing antibiotic resistance in the environment.

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