Abstract
To understand the characteristics of bacterial viability and diversity in landscape waters replenished with reclaimed water, the typical landscape lake using reclaimed water was investigated in this study. Samples were collected from a reclaimed water inlet (P1), a reclaimed water distribution outlet (P2), and a landscape lake replenished by reclaimed water (P3). By means of measuring adenosine triphosphate (ATP), flow cytometry (FCM), and 16S rRNA gene high-throughput sequencing, the bacterial viability and diversity in reclaimed water distribution system and landscape lake were illustrated. The bacterial ATP contents at P1, P2, and P3 were 3.55 ± 1.79 ng/L, 3.31 ± 1.43 ng/L, and 18.97 ± 6.39 μg/L, and the intact bacterial cell concentrations were 5.91 ± 0.52 × 104 cells/mL, 7.95 ± 2.58 × 104 cells/mL, and 5.65 ± 2.10 × 106 cells/mL, respectively. These results indicated a significant increase of bacterial viability in the landscape lake. The Shannon diversity index of 6.535, 7.05, and 6.886 at P1, P2, and P3, respectively, demonstrated no notable change of bacterial diversity from reclaimed water distribution system to landscape lake. However, the relative abundance of Pseudomonas sp. at P3 was significantly higher than that at P1. These findings indicated that viable but non-culturable (VBNC) bacteria could be revived in the landscape lake. The bacterial viability during reclaimed water reuse should deserve special attention.
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References
Achtman M, Wagner M (2008) Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6:431–440
Blatchleyiii ER, Cullen JJ, Petri B, Bircher KG, Welschmeyer NA (2018) The biological basis for ballast water performance standards: “viable/non-viable” or “live/dead”? Environ Sci Technol 52:8075–8086
Buse HY, Ashbolt NJ (2012) Counting Legionella cells within single amoeba host cells. Appl Environ Microbiol 78:2070–2072
Cai L, Zhang T (2013) Detecting human bacterial pathogens in wastewater treatment plants by a high-throughput shotgun sequencing technique. Environ Sci Technol 47:5433–5441
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Casero MC, Velazquez D, Medinacobo M, Quesada A, Cires S (2019) Unmasking the identity of toxigenic cyanobacteria driving a multi-toxin bloom by high-throughput sequencing of cyanotoxins genes and 16S rRNA metabarcoding. Sci Total Environ 665:367–378
Chen R, Ao D, Ji J, Wang XC, Li YY, Huang Y, Xue T, Guo H, Wang N, Zhang L (2017) Insight into the risk of replenishing urban landscape ponds with reclaimed wastewater. J Hazard Mater 324:573–582
Cho M, Kim J, Kim JY, Yoon J, Kim JH (2010) Mechanisms of Escherichia coli inactivation by several disinfectants. Water Res 44:3410–3418
Coggins LX, Larma I, Hinchliffe A, Props R, Ghadouani A (2020) Flow cytometry for rapid characterisation of microbial community dynamics in waste stabilisation ponds. Water Res 169:115–243
Collier SA, Stockman LJ, Hicks LA, Garrison LE, Zhou FJ, Beach MJ (2012) Direct healthcare costs of selected diseases primarily or partially transmitted by water. Epidemiol Infect 140:2003–2013
D’Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E, Epstein S, Clardy J, Lewis K (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17:254–264
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998
Egli T (2010) How to live at very low substrate concentration. Water Res 44:4826–4837
Garner E, Mclain JET, Bowers J, Engelthaler DM, Edwards M, Pruden A (2018) Microbial ecology and water chemistry impact regrowth of opportunistic pathogens in full-scale reclaimed water distribution systems. Environ Sci Technol 52:9056–9068
Gosling SN, Arnell NW (2016) A global assessment of the impact of climate change on water scarcity. Clim Chang 134:371–385
Hammes F, Goldschmidt F, Vital M, Wang Y, Egli T (2010) Measurement and interpretation of microbial adenosine tri-phosphate (ATP) in aquatic environments. Water Res 44:3915–3923
Hu M, Wang X, Wen X, Xia Y (2012) Microbial community structures in different wastewater treatment plants as revealed by 454-pyrosequencing analysis. Bioresour Technol. Bioresour Technol 117:72–79
Jjemba PK, Weinrich LA, Cheng W, Giraldo E, Lechevallier MW (2010) Regrowth of potential opportunistic pathogens and algae in reclaimed-water distribution systems. Appl Environ Microbiol 76:4169–4178
Jjemba PK, Johnson W, Bukhari Z, Lechevallier MW (2015) Occurrence and control of Legionella in recycled water systems. Pathogens 4:470–502
Kim CJ, Kim NH, Song KH, Choe PG, Kim ES, Park SW, Kim HB, Kim NJ, Kim EC, Park WB (2013) Differentiating rapid- and slow-growing mycobacteria by difference in time to growth detection in liquid media. Diagn Microbiol Infect Dis 75:73–76
Lautenschlager K, Hwang C, Liu WT, Boon N, Köster O, Vrouwenvelder H, Egli T, Hammes F (2013) A microbiology-based multi-parametric approach towards assessing biological stability in drinking water distribution networks. Water Res 47:3015–3025
Limayem A, Wasson S, Mehta M, Pokhrel AR, Patil S, Nguyen M, Chen J, Nayak B (2019) High-throughput detection of bacterial community and its drug-resistance profiling from local reclaimed wastewater plants. Front Cell Infect Microbiol 9:303
Lin W, Yu Z, Zhang H, Thompson IP (2014) Diversity and dynamics of microbial communities at each step of treatment plant for potable water generation. Water Res 52:218–230
Lin Y, Li D, Gu AZ, Zeng S, He M (2016a) Bacterial regrowth in water reclamation and distribution systems revealed by viable bacterial detection assays. Chemosphere 144:2165–2174
Lin Y, Li D, Zeng S, He M (2016b) Changes of microbial composition during wastewater reclamation and distribution systems revealed by high-throughput sequencing analyses. Front Environ Sci Eng 10:539–547
Ma XY, Wang XC, Wang D, Ngo HH, Zhang Q, Wang Y, Dai D (2016) Function of a landscape lake in the reduction of biotoxicity related to trace organic chemicals from reclaimed water. J Hazard Mater 318:663–670
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963
Mccarty PL, Jaeho B, Jeonghwan K (2011) Domestic wastewater treatment as a net energy producer-can this be achieved? Environ Sci Technol 45:7100–7106
Michael-Kordatou I, Michael C, Duan X, He X, Dionysiou DD, Mills MA, Fatta-Kassinos D (2015) Dissolved effluent organic matter: characteristics and potential implications in wastewater treatment and reuse applications. Water Res 77:213–248
Ministry of Water Resources (MWR) (2006) Standards of reclaimed water quality SL368–2006. Beijing (in Chinese)
Nescerecka A, Rubulis J, Vital M, Juhna T, Hammes F (2014) Biological instability in a chlorinated drinking water distribution network. PLoS One 9:96354
Oliveira MC, Repetti SI, Iha C, Jackson CJ, Díaz-Tapia P, Lubiana KMF, Cassano V, Costa JF, Cremen MCM, Marcelino VR (2018) High-throughput sequencing for algal systematics. Eur J Phycol 53:256–272
Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415–425
Omidbakhsh N (2010) Evaluation of sporicidal activities of selected environmental surface disinfectants: carrier tests with the spores of Clostridium difficile and its surrogates. Am J Infect Control 38:718–722
Pattison DI, Davies MJ (2012) Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds. Chem Res Toxicol 14:1453–1464
Pinto AJ, Xi C, Raskin L (2012) Bacterial community structure in the drinking water microbiome is governed by filtration processes. Environ Sci Technol 46:8851–8859
Prest EI, Hammes F, Kötzsch S, van Loosdrecht MCM, Vrouwenvelder JS (2013) Monitoring microbiological changes in drinking water systems using a fast and reproducible flow cytometric method. Water Res 47:7131–7142
Prest EI, El-Chakhtoura J, Hammes F, Saikaly PE, van Loosdrecht MCM, Vrouwenvelder JS (2014) Combining flow cytometry and 16S rRNA gene pyrosequencing: a promising approach for drinking water monitoring and characterization. Water Res 63:179–189
Prest EI, Weissbrodt DG, Hammes F, Loosdrecht MCMV, Vrouwenvelder JS (2016) Long-term bacterial dynamics in a full-scale drinking water distribution system. PLoS One 11:0164445
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596
Riemann BO (1979) The occurrence and ecological importance of dissolved ATP in fresh water. Freshw Biol 9:481–490
State Environmental Protection Administration (SEPA) (2006) Water and wastewater monitoring method, 4th edn. China Environmental Science Press, Beijing (in Chinese)
Teklehaimanot GZ, Genthe B, Kamika I, Momba MNB (2015) Prevalence of enteropathogenic bacteria in treated effluents and receiving water bodies and their potential health risks. Sci Total Environ 518-519:441–449
Thayanukul P, Kurisu F, Kasuga I, Furumai H (2013) Evaluation of microbial regrowth potential by assimilable organic carbon in various reclaimed water and distribution systems. Water Res 47:225–232
Thomas V, Loret JF, Jousset M, Greub G (2008) Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. Environ Microbiol 10:2728–2745
Van Nevel S, Buysschaert B, De Gusseme B, Boon N (2016) Flow cytometric examination of bacterial growth in a local drinking water network. Water Environ J 30:167–176
Van Nevel S, Koetzsch S, Proctor CR, Besmer MD, Prest EI, Vrouwenvelder JS, Knezev A, Boon N, Hammes F (2017) Flow cytometric bacterial cell counts challenge conventional heterotrophic plate counts for routine microbiological drinking water monitoring. Water Res 113:191–206
Vila-Costa M, Gasol JM, Sharma S, Moran MA (2012) Community analysis of high- and low-nucleic acid-containing bacteria in NW Mediterranean coastal waters using 16S rDNA pyrosequencing. Environ Microbiol 14:1390–1402
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Wang Y, Hammes F, Egli T (2008) The impact of industrial-scale cartridge filtration on the native microbial communities from groundwater. Water Res 42:4319–4326
Wang Y, Hammes F, Roy KD, Verstraete W, Boon N (2010) Past, present and future applications of flow cytometry in aquatic microbiology. Trends Biotechnol 28:416–424
Wang XC, Zhang C, Ma X, Luo L (2015) Water cycle management-a new paradigm of wastewater reuse and safety control. Springer briefs in water science and technology
Wielen PWJJ, van der Kooij D (2010) Effect of water composition, distance and season on the adenosine triphosphate concentration in unchlorinated drinking water in the Netherlands. Water Res 44:4860–4867
Williams K, Pruden A, Falkinham J, Edwards M (2015) Relationship between organic carbon and opportunistic pathogens in simulated glass water heaters. Pathogens 4:355–372
Xu L, Zhang C, Xu P, Wang XC (2017) Mechanisms of ultraviolet disinfection and chlorination of Escherichia coli: culturability, membrane permeability, metabolism, and genetic damage. J Environ Sci 65:356–366
Yang Y, Gu X, Te SH, Goh SG, Mani K, He Y, Gin KY (2019) Occurrence and distribution of viruses and picoplankton in tropical freshwater bodies determined by flow cytometry. Water Res 149:342–350
Zhang S, Huang Z, Lu S, Zheng J, Zhang X (2017) Nutrients removal and bacterial community structure for low C/N municipal wastewater using a modified anaerobic/anoxic/oxic (mA2/O) process in North China. Bioresour Technol 243:975–985
Zhou J, Wang XC, Ji Z, Xu L, Yu Z (2015) Source identification of bacterial and viral pathogens and their survival/fading in the process of wastewater treatment, reclamation, and environmental reuse. World J Microbiol Biotechnol 31:109–120
Zipper H, Brunner H, Bernhagen J, Vitzthum F (2004) Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications. Nucleic Acids Res 32:103h
Funding
This work was supported by the National Natural Science Foundation of China (No. 51578441), the National Program of Water Pollution Control (No. 2013ZX07310-001), and the Key Research and Development Project of Shaanxi Province (No.2020ZDLNY06-07).
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Highlights
• Bacterial viability and diversity were investigated in the landscape reuse system
• Bacterial viability increased greatly in the landscape lake
• VBNC bacteria obviously revived when replenishing the landscape lake
• Bacterial diversity changes slightly except several phyla and genus
Main finding
VBNC bacteria revived during replenishing of a landscape lake, while bacterial diversity showed no great change.
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Bacterial viability and diversity in a landscape lake replenished with reclaimed water: a case study in Xi’an, China (DOCX 29 kb).
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Zhang, C., Xu, P., Wang, X.C. et al. Bacterial viability and diversity in a landscape lake replenished with reclaimed water: a case study in Xi’an, China. Environ Sci Pollut Res 27, 32796–32808 (2020). https://doi.org/10.1007/s11356-020-08910-1
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DOI: https://doi.org/10.1007/s11356-020-08910-1