Article pubs.acs.org/est
Microbial Community Response to Chlorine Conversion in a Chloraminated Drinking Water Distribution System Hong Wang,† Caitlin R. Proctor,† Marc A. Edwards,† Marsha Pryor,‡ Jorge W. Santo Domingo,§ Hodon Ryu,§ Anne K. Camper,∥ Andrew Olson,∥ and Amy Pruden†,* †
Via Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, Virginia 24061, United States Pinellas County Utilities Laboratory, Largo, Florida 33778, United States § U.S. Environmental Protection Agency, Cincinnati, Ohio 45220, United States ∥ Center for Biofilm Engineering, Montana State University, Bozeman, Montana 59717, United States ‡
S Supporting Information *
ABSTRACT: Temporary conversion to chlorine (i.e., “chlorine burn”) is a common approach to controlling nitrification in chloraminated drinking water distribution systems, yet its effectiveness and mode(s) of action are not fully understood. This study characterized occurrence of nitrifying populations before, during and after a chlorine burn at 46 sites in a chloraminated distribution system with varying pipe materials and levels of observed nitrification. Quantitative polymerase chain reaction analysis of gene markers present in nitrifying populations indicated higher frequency of detection of ammonia oxidizing bacteria (AOB) (72% of samples) relative to ammonia oxidizing archaea (AOA) (28% of samples). Nitrospira nitrite oxidizing bacteria (NOB) were detected at 45% of samples, while presence of Nitrobacter NOB could not be confirmed at any of the samples. During the chlorine burn, the numbers of AOA, AOB, and Nitrospira greatly reduced (i.e., 0.8−2.4 log). However, rapid and continued regrowth of AOB and Nitrospira were observed along with nitrite production in the bulk water within four months after the chlorine burn, and nitrification outbreaks appeared to worsen 6−12 months later, even after adopting a twice annual burn program. Although high throughput sequencing of 16S rRNA genes revealed a distinct community shift and higher diversity index during the chlorine burn, it steadily returned towards a condition more similar to pre-burn than burn stage. Significant factors associated with nitrifier and microbial community composition included water age and sampling location type, but not pipe material. Overall, these results indicate that there is limited long-term effect of chlorine burns on nitrifying populations and the broader microbial community.
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INTRODUCTION Drinking water distribution systems (DWDSs) are becoming recognized as a key microbial habitat that is shaped by engineering factors.1−5 In the U.S. and other countries, many water utilities have switched from chlorine to chloramines for secondary disinfection of drinking water, primarily to reduce concentrations of disinfection byproducts.6 However, chloramination can trigger undesirable nitrification, leading to increased nitrite and nitrate concentrations, faster chloramine decay, microbial proliferation, and decreased pH and dissolved oxygen in distributed water.7,8 Nitrification can also influence corrosion, sometimes increasing release of lead and copper to water supplies8−10 and there is concern about other health and aesthetic issues.11 Nitrification occurred in 63% of U.S. medium and large water systems performing chloramination, posing a challenge for meeting targeted levels of disinfectant residuals in distribution systems.12 Nitrification is a two-step biological process that converts ammonia to nitrite by ammonia oxidizing bacteria (AOB) and further to nitrate by nitrite oxidizing bacteria (NOB).11 The © 2014 American Chemical Society
intermediate nitrite can also be oxidized by chloramine in drinking water, which in turn accelerates chloramine decay.13 Common genera of AOB and NOB in drinking water systems include Nitrosomonas, Nitrosospira, Nitrobacter, and Nitrospira.14−16 Two recent studies also reported a significant role of ammonia oxidizing archaea (AOA) in water treatment plant biofilters.15,17 However, the occurrence and exact role of nitrifiers appears to vary from case to case.14,15,17−20 Short-term switching to chlorine as the secondary disinfectant (i.e., “chlorine burn”) is a common approach for nitrification control in chloraminated distribution systems.7,21 However, the exact effect of chlorine burns on nitrifying populations and the broader microbial community, as well as practical effectiveness for nitrification control, is not wellestablished. Carrico et al.21 reported reoccurrence of Received: Revised: Accepted: Published: 10624
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chromatograph (Dionex, Sunnyvale, CA) according to EPA method 300.0.24 Water Sample Processing and DNA Extraction. Twoand-a-half-liter water samples were filtered through 0.22 μmpore-size mixed cellulose ester filters (Millipore, Billerica, MA), which were fragmented using sterile tweezers and placed in 2 mL Lysing Matrix A tubes (MP Biomedicals, Solon, OH). These tubes were shipped overnight on dry ice for DNA extraction using a FastDNA SPIN Kit (MP Biomedicals) according to manufacturer protocol. Quantitative Polymerase Chain Reaction (qPCR). AOB, AOA, Nitrospira, Nitrobacter, and total bacteria were enumerated by qPCR by targeting ammonia monooxygenase (amoA)25,26 or corresponding 16S rRNA27−29 genes (Supporting Information (SI) Table S1). All qPCR reactions were performed in triplicate in a 10 μL system containing 1 × SsoFast Probes or Evagreen supermix (Bio-Rad, Hercules, CA), 250 or 400 nM primers, 93.75 nM probe (Nitrobacter Taqman assay only), and 1 μL template. Samples were diluted at 1:10 or 1:100 ratios to minimize PCR inhibition.30 DNA extracts, negative control (sterilized nanopure water) and 10-fold serial dilutions of positive standards (PCR products amplified from plasmid clones) were included in each qPCR run. Melt curve analyses were performed for each Evagreen assay for end-point examination of PCR product specificity. The limits of quantification (LOQ) were 10 gene copies/reaction for AOB, Nitrobacter, and Nitrospira assays and 100 gene copies/reaction for the AOA assay. The r2 of calibration curves were >0.99 and standard deviations of threshold cycle (Ct) values at the LOQ were 10 6 16S rRNA gene copies/mL during the 9-month investigation (Figure 1). Chlorine burn greatly decreased the
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RESULTS Water Chemistry in the Distribution System. The average nitrite concentration across the 46 sites (Table 1) decreased from 0.16 ± 0.11 mg/L during the Preburn stage to 0.01 ± 0.02 mg/L during the immediately after-burn stage (P < 0.05). However, a slight increase in nitrite level was noted 4months after the chlorine burn (P < 0.05), though it was still lower than the Preburn stage (P < 0.05). The number of sites with nitrite concentration ≥0.05 mg/L (a generally accepted indicator of nitrification outbreak) decreased from 37 to 2 from preburn to immediately after burn, but then increased to 9 positive sites 4 m after-burn. Nitrate variation exhibited a similar trend as nitrite (Table 1). In contrast, free and total ammonia concentrations continued to increase after the chlorine burn (P < 0.05). Total chloramine residuals after the chlorine burn were significantly higher than the Preburn (P < 0.05), while there was no difference between Immediately afterburn and 4 month-after-burn stages (P > 0.05). Temperature during the Immediately after-burn stage was slightly lower (P < 0.05), decreasing to 21.8 ± 1.5 °C during the winter season when the fourth sampling occurred. A slight increase in pH was observed after chlorine burn (P < 0.05). According to principle component analysis, PC1 and PC2 explained 67.8% of the total physiochemical data variance of water samples in Preburn, Immediately after-burn, and 4 mafter-burn stages (SI Figure S1). Samples from different stages were mainly clustered along PC1, which was driven by nitrite, nitrate, temperature, and turbidity along the positive axis and
Figure 1. Effect of chlorine burn on 16S rRNA gene copies in the drinking water distribution system. Samples were collected from 46 sites prior to (Preburn), during (Burn), immediately after (Immediately after burn) and 4 m after (4 m after burn) switching from chloramines to chlorine as the secondary disinfectant. The bottom, middle and top line of the box correspond to the 25%, 50%, and 75% percentiles, respectively. The upper and lower whisker extend to the highest or lowest value within 1.5 × IQR (interquartile range), respectively. Data beyond the end of the whiskers are outliers and plotted as points.
bulk water bacterial densities (average reduction = 1.7 log, P < 0.05), although densities increased once the system was switched back to chloramination (P < 0.05). A continuous increase was observed (P < 0.05), even during the winter, resulting in a similar level of total bacteria 4 m after-burn compared to Preburn (P = 1). Effect of Chlorine Burn on AOA, AOB, Nitrospira, and Nitrobacter. AOB were detected in 72% of all water samples (n = 184), ranging from 0.05 mg-N/L NO3− after the chlorine burn illustrates the effectiveness of switching to chlorine upon nitrification onset, but there is evidence that the effects are only short-term. Gene copies corresponding to nitrifiers (i.e., AOB, Nitrospira) quickly recovered, suggesting survival of nitrifiers through the chlorine burn and a restored nitrification potential within a short time frame. This is consistent with a DWDS simulation study that reported survival of AOB through chlorine treatments once they were established as part of the pipe biofilm.40 Presence of AOB was also observed on a distribution pipe specimen using fluorescence in situ hybridization in one DWDS that converted from chloramination to chlorination.21 Lee et al.41 reported limited free chlorine penetration in drinking water nitrifying biofilm, which might explain incomplete inactivation of nitrifiers by chlorine. Moreover, repeated chlorine burns could potentially select for chlorine-resistant nitrifiers, which might shorten the chlorine burn effectiveness period. Despite increasing to two burns per year subsequent to this study (i.e., May−June and September, 2013), elevated nitrite levels indicated that nitrification returned within two months of each burn (SI Figure S3). Physiochemical Factors Associated with Nitrification. The optimal temperature for nitrifier growth in drinking water has been reported to range from 25 to 30 °C;11 however, nitrifiers can survive and nitrification can ensue at much lower temperatures (e.g., 6 °C).12,42−44 Weak association between temperature and nitrifier gene copies is likely due to the narrow temperature range over the period of this study (20−30 °C). Even in winter, the temperature of the distributed water was about 20 °C, which still poses a challenge for nitrification control. Negative correlation between temperature and total chlorine (SI Table S3) implies a synergistic effect of these two factors for controlling nitrification. Negative correlation between cultivable nitrifying bacteria and total chlorine concentration was observed in Finnish drinking water samples.42 A pilot scale study showed absence of nitrification when total chlorine was >2.2 mg/L,45 which is in agreement with our findings of low nitrification occurrence rates for average total chlorine concentration of >2 mg/L following the chlorine burn. However, survival of nitrifiers has been reported in chloraminated water with >5 mg/L chloramine.46 Positive associations between nitrifying groups and nitrite/ nitrate concentration, as well as negative associations between nitrifiers and ammonia concentration, illustrate that AOA, AOB, and Nitrospira gene copies rise accordingly with nitrification outbreak. Although high pH is known to negatively influence nitrification,47 the negative association between pH and nitrifiers observed in this study is more likely a result of interrelationships among multiple physiochemical factors, since pH remained within an optimal range for nitrifier growth (i.e., 7.07−7.98). Microbial Community Composition of the DWDS. Dominance of γ-Proteobacteria in PCF chloraminated water was in contrast to several previous high throughput sequencing studies reporting overall dominance of α-Proteobacteria and/or β-Proteobacteria in chloraminated DWDSs,2,4,35,48 including pyrosequencing profiling of water samples from one PCF groundwater treatment plant (this plant served as source water for the 100% groundwater POE site in the present study).35 However, high abundance of γ-Proteobacteria was found in two 10630
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and lead, but have difficulty surviving on new copper pipes.8 The difference might be attributed to age of pipes, different configurations and physiochemical conditions in DWDSs, for example, higher surface area to volume ratio is a hallmark of building plumbing relative to DWDSs.58 Variation of microbial community structure among different sampling sites illustrates the importance of selection of drinking water quality monitoring points. Permanent compliance sites (i.e., BAC sites) for regular drinking water monitoring are usually located in closer proximity to the larger main lines; while BO sites are mostly in low flow areas and near the ends of the streets. Separation of BAC sites and BO sites (Figure 5) illustrated routine monitoring of permanent compliance sites does not reflect conditions encountered at the distal ends of distribution systems. Autoflushing devices (AFD), mainly used for sediment and biofilm removal, are usually installed in places with nitrification problems. Similar clustering of AFD sites and BAC sites implies effectiveness of autoflushing in replenishing fresh water to nitrification sites, which theoretically can shorten water age and help mitigate nitrification. Skadsen et al.7 reported association between nitrification and discontinued hydrant flushing. Insights into Drinking Water System Nitrification Control and Research Needs. This study provides a quantitative estimation of the response of drinking water nitrification biomarkers to chlorine burn applied in response to a real-world nitrification outbreak. Rapid regrowth of AOB and Nitrospira within a month and continued growth thereafter implies that long-term effectiveness of chlorine burn toward nitrification control may be limited. Though chemical evidence of nitrification is still improved four months after chlorine burn relative to preburn, this study suggests that the trigger is in place for outbreak once favorable growth conditions are again met for nitrifying microorganisms. Further studies on the longterm practical effectiveness of chlorine burns for nitrification control would be of value, particularly in terms of clarifying the role of temperature as a seasonal covariate. Studies investigating the potential for chlorine burn to select for chlorine-resistant nitrifiers are especially of interest. Overall, the results of this study provide insight into the effect of chlorine burn on inactivation of nitrifying populations and the broader microbial community in a full-scale distribution system. This can assist in formulating practical guidance for drinking water utilities in terms of selection and optimization of nitrification control strategies.
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Article
AUTHOR INFORMATION
Corresponding Author
*Phone: (540) 231-3980; fax: (540) 231-7916; e-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS Funding was provided in part by the Alfred P. Sloan Foundation Microbiology of the Built Environment Program, the U.S. National Science Foundation CBET Award No. 1033498, and student fellowships supported by the Sussman Foundation and Pinellas County. Additionally, the U.S. Environmental Protection Agency, through its Office of Research and Development and the RARE program, funded in part and collaborated in the research described herein. We also thank Fred Small of Pinellas County Florida for assisting with sampling and data logging and Michael Elk for technical assistance.
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ASSOCIATED CONTENT
S Supporting Information *
includes qPCR assay oligonucleotides and conditions (Table S1), validation of qPCR assay specificity (Table S2), correlation analysis of water chemistry parameters during chloramination (Table S3), ANOSIM analysis of microbial community at different stages (Table S4), The most abundant phyla, classes, families and genera in water samples at different stages (Table S5), Principal component analysis of water physiochemical properties during chloramination (Figure S1), multidimensional scaling analysis of microbial community color coded by sampling location types (Figure S2), and field nitrite concentration after chlorine burns in 2013 (Figure S3) . This material is available free of charge via the Internet at http:// pubs.acs.org. 10631
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