Drivers of Staphylococcus aureus dynamics and survival in recreational waters

Abstract

Staphylococcus aureus is the leading cause of bacterial fatalities worldwide. Previously only an issue in health-care settings, the rise of community-acquired (CA) S. aureus infections has become a global health concern. Investigating S. aureus in the environment, such as recreational waters, has become a crucial area of research to prevent CA-S. aureus infections since heightened recreational water activity is correlated to higher rates of S. aureus infections. Despite this known elevated risk of S. aureus infection after swimming, many impacts of physicochemical and environmental factors on the distribution, abundance, and persistence of S. aureus in fresh, estuarine, and marine waters are still unknown. The purpose of this dissertation is to model the abundance, virulence, and survival of S. aureus in diverse aquatic environments by integrating high resolution spatial and temporal environmental data with experimental mesocosms and advanced statistical approaches to create predictive mixed effects models. My overarching hypothesis is that physicochemical factors associated with increased anthropogenic influences will be significantly predictive of increased S. aureus concentrations and survival. High spatial and temporal sampling of a marine system, detected S. aureus, methicillin-resistant S. aureus (MRSA), and fecal indicator bacteria (FIB) in seawater and sand using standard microbial culturing techniques, with the highest concentrations observed at beaches with freshwater input and during conditions of elevated water turbidity. The results from predictive generalized linear models (GLM) and generalized linear mixed models (GLMM) also revealed elevated bacterial concentrations at beaches with higher densities of on-site sewage disposal systems (OSDS). Notably, the predictive models developed herein are for practical application, representing the first of their kind in predicting S. aureus and MRSA presence in recreational waters. These data underscore the importance of freshwater, especially surface waters, as potential sources of S. aureus and MRSA. Expanding on these findings, we utilized culture-based and molecular methods to detect and model S. aureus, including the identification of antibiotic-resistant and virulent S. aureus genes across multiple seasons to determine environmental predictors across a watershed level gradient. GLM and GLMM show seasonal and spatial variations in S. aureus concentrations, highlighting method-dependent differences and uncovering potential sources of antibiotic-resistant and virulent S. aureus strains, including human and zoonotic origins. Furthermore, we investigated the potential link between turbidity and enhanced S. aureus survival. This was tested through a microcosm incubation using unfiltered fresh and brackish water samples. GLMM analysis and decay calculations revealed that salinity and turbidity were significant predictors of environmental S. aureus concentrations, showing the lowest decay rates in brackish, highly turbid microcosms. This suggests that saline and turbid environments, particularly in the absence of sunlight, create favorable conditions for the prolonged persistence of S. aureus communities. Overall, many physicochemical factors, especially those linked to increased anthropogenic influences (e.g., turbidity, OSDS, human shedding) were found as significant predictors of heightened S. aureus concentrations and survival. Collectively, these chapters provide a comprehensive examination of S. aureus dynamics in different aquatic settings, offering valuable insights for water quality management and public health interventions to mitigate the impact of S. aureus in recreational waters.