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Spatiotemporal trends in particle-associated microbial communities in a chlorinated drinking water distribution system [1]

['Madison Ferrebee', 'Wadsworth Department Of Civil', 'Environmental Engineering', 'West Virginia University', 'Morgantown', 'West Virginia', 'United States Of America', 'Erika Osborne', 'Emily Garner']

Date: 2023-12

Various spatiotemporal, hydraulic, and water quality parameters can affect the microbial community composition of water within drinking water distribution systems (DWDSs). Although some relationships between various paravmeters and microbial growth are known, the effects of spatial and temporal trends on particle-associated microbial communities in chlorinated DWDSs remain poorly understood. The objectives of this study were to characterize the microbial community composition of both particle-associated bacteria (PAB) and total bacteria (TB) within a full-scale chlorinated DWDS, and assess relationships between microbiavvl community and various spatiotemporal, hydraulic, and water quality parameters. Bulk water samples were collected from the treatment plant, a storage tank, and 12 other sites in a rural chlorinated DWDS at varying distances from the treatment plant on four sampling dates spanning six months. Amplicon sequencing targeting the 16S rRNA gene was performed to characterize the microbial community. Gammaproteobacteria dominated the DWDS, and hydraulic parameters were well-correlated with differences in microbial communities between sites. Results indicate that hydraulic changes may have led to the detachment of biofilms and loose deposits, subsequently affecting the microbial community composition at each site. Spatial variations in microbial community were stronger than temporal variations, differing from similar studies and indicating that the highly varied hydraulic conditions within this system may intensify spatial variations. Genera containing pathogenic species were detected, with Legionella and Pseudomonas detected at every site at least once and Mycobacterium detected at most sites. However, only one sample had quantifiable Pseudomonas aeruginosa through quantitative polymerase chain reaction (qPCR), and no samples had quantifiable Legionella pneumophila or Mycobacterium avium, indicating a low human health risk. This study establishes spatial variations in PAB associated with varied hydraulic conditions as an important factor driving microbial community within a chlorinated DWDS.

Funding: This project was funded in part by the West Virginia University (WVU) Research Office via the Faculty Research and Scholarship Advancement Grant (to EG) and the National Science Foundation (NSF; award 2238953 to EG). Additionally, this material is based upon work supported by the NSF Graduate Research Fellowship Program (award 2136524 to MF). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of NSF. Computational resources were provided by the WVU Research Computing Spruce Knob high performance computing cluster, which is funded in part by NSF EPS-1003907. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

1. Introduction

In the United States, the quality of drinking water is regulated by the Safe Drinking Water Act, along with state and local guidelines. The majority of regulations focus on drinking water leaving the treatment plant; however, the quality of drinking water may change as it travels from the treatment plant through the drinking water distribution system (DWDS) to consumers’ taps. Many factors can influence water quality throughout DWDSs, including the presence of disinfectant residual [1–4], microbial growth and biofilm formation [5–7], the accumulation and transport of sediments and loose deposits [8–10], hydraulics and stagnation [10–12], pipe size and material [13, 14], and various spatial and temporal influences [8, 10, 15–18].

Bacteria can survive treatment and enter DWDSs or enter through intrusion or maintenance work on the system. To prevent the presence of bacteria, treatment facilities often maintain a disinfectant residual, such as chlorine or chloramine, within DWDSs. In the United States, a disinfectant residual is required [19]. However, biofilms that grow on pipe walls and sediments can create habitats for bacteria to grow, protected from disinfectants. Bacteria and biofilms exert a demand on disinfectant residual, further creating an environment suitable for bacterial growth. Other compounds present in DWDSs, such as corrosion products, can also react with disinfectants and decrease disinfectant residual [19], allowing for more bacterial growth. Just as the absence of disinfectant residual can create health concerns, so can its presence. Disinfectants can react with organic materials within DWDSs to create disinfection byproducts, such as trihalomethanes and haloacetic acids [20], some of which have been linked to cancer and reproductive effects [21].

Previous studies have attempted to draw relationships between various parameters and microbial community composition within DWDSs. Potgieter et al. [18] found that spatial dynamics were stronger than temporal when considering a DWDS using multiple disinfection strategies throughout the system, but temporal dynamics were stronger within each disinfection section. Other studies have also found strong temporal variations in microbial community throughout DWDSs [16, 17]. Sekar et al. [22] found that cells attach to DWDS pipes during low flow periods and mobilize during active flow periods, influencing daily and weekly patterns of bacterial abundance based on periods of high and low demand. Douterelo et al. [11] found that hydraulic conditions can cause changes to the composition and structure of microbial communities within biofilms and bulk water. Relationships between microbial community and various water quality parameters, such as chlorine residual, temperature, pH, and metal concentrations [16, 18, 23], have been studied in the past, but considerable variation between systems has been documented. These variations between systems indicate that the factors affecting microbial community in DWDSs are complex and vary based on multiple system-specific characteristics.

While the effect of biofilms growing on pipe walls on microbial community has been extensively studied, the effect of biofilms growing on sediments and other suspended particles is largely unknown [24, 25]. Liu et al. [6] found that over 98% of total bacteria within an unchlorinated DWDS were found within the pipe wall biofilm and loose deposits, with loose deposits contributing more biomass to the system than biofilm. Van der Wielen and Lut [26] found that sediment-associated biofilms in DWDSs are an important contributor to microbial community. To prevent the buildup of sediments within DWDSs, some utilities apply a flushing routine, where high-flow velocities are applied throughout the DWDS to disturb, resuspend, and remove particles from the system [27]. However, these practices have been found to sometimes increase the quantity of bacteria within the system. Osborne et al. [10] found that after flushing, the concentration of total suspended solids (TSS) decreased in a storage tank but the concentration of particle-associated bacteria (PAB) increased throughout the DWDS, suggesting that bacteria associated with sediments from the tank may have been resuspended and redistributed as a result of flushing. El-Chakhtoura et al. [9] also found that flushing increases biomass within DWDSs due to the resuspension of pipe biofilm and loose deposits.

Chen et al. [8] recently published a paper in which differences between planktonic bacteria and PAB were studied in an unchlorinated DWDS. The study found planktonic bacteria and PAB from produced water were the main contributors to bacteria within the DWDS, and that the influence of biofilm and loose deposits to the planktonic bacteria and PAB was the highest during daily demand peaks. However, this study did not capture variations over multiple sampling events and included limited sampling points to capture spatial variations. Additionally, the study was on an unchlorinated system and the authors expressed the need for future study of chlorinated systems to better understand particle-associated microbiology within DWDSs. Osborne et al. [10] demonstrated that biofilms formed on particles represented a substantial portion of overall microbial loading within a DWDS. The current study expands upon this research to establish which bacteria are present and associated with particles, and to determine any potential human health risk.

Although many bacteria that grow within DWDSs are not harmful to human health and may actually help select against pathogens [28], opportunistic pathogens (OPs), such as Legionella pneumophila, Pseudomonas aeruginosa, and Mycobacterium avium, can inhabit DWDSs and premise plumbing, causing health effects such as Legionnaires’ disease, pneumonia, and nontuberculous Mycobacteria infections [29]. These OPs can thrive even in the presence of disinfectant residual [30, 31] and are the leading cause of waterborne disease outbreaks in developed countries [32]. An estimated 7.15 million waterborne illnesses occur annually in the United States, causing 118,000 hospitalizations, 6,630 deaths, and approximately $3.33 billion in healthcare costs [33]. The majority of hospitalizations and deaths are caused by biofilm-associated OPs (L. pneumophila, P. aeruginosa, nontuberculous mycobacteria) [33]. It is therefore important to understand relationships between microbial community and various spatiotemporal, hydraulic, and water quality factors to prevent the growth of harmful organisms and ensure the safety of consumers.

While numerous studies have attempted to establish relationships between various parameters and microbial growth, as summarized above, the effects of spatial and temporal trends on particle-associated microbial communities in chlorinated DWDSs remain poorly understood. The objectives of this study were to 1) examine the microbial community composition within a full-scale chlorinated DWDS, 2) explore relationships between microbial community and various spatiotemporal, hydraulic, and water quality parameters, 3) investigate how sediment may be a driver of these relationships through examining both particle-associated bacteria (PAB) and total bacteria (TB), and 4) establish potential human health implications of bacteria within the DWDS. Amplicon sequencing targeting the 16S rRNA gene was performed to characterize the microbial community of bulk water from the treatment plant, a storage tank, and 12 other sites throughout a chlorinated drinking water distribution system. Analyses were separated into both PAB and TB for each sample, and results were compared to various physicochemical and hydraulic parameters. The results from this study will inform treatment plant operators on the effects particles can have on microbial community, helping shape treatment and management techniques to improve the biological water quality of drinking water throughout DWDSs.

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[1] Url: https://journals.plos.org/water/article?id=10.1371/journal.pwat.0000183

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