The variation of microbiological characteristics in surface waters during persistent precipitation

Highlights

● The maximum coliforms concentration increased by 2 Logs during rainfall.

● Culturable bacterial concentrations had a delayed increase during precipitation.

● DOC concentration was the main impact factor for the microbial characteristics.

● Culturable bacteria concentrations in waters could recover to pre-rainfall levels.

Abstract

Climate change leads to an increase in both the frequency and intensity of extreme precipitation. Surface runoff generated by extreme precipitation has a significant impact on water. However, the impact of persistent precipitation on surface water quality is easy to neglect, due to its prolonged duration and lower-intensity rainfall. This study established eight sampling points within selected surface waters to observe the variation of microbial characteristics in a typical persistence precipitation event. The primary difference between Furong Lake (FL) and Chengqian Reservoir (CR) was: the concentrations of dissolved organic carbon (DOC) were 21.3 ± 0.7 and 8.3 ± 1.5 mg/L in FL and CR, respectively. The concentrations of R2A culturable bacteria and coliforms were 10^4.57 and 10^1.58 colony-forming units (CFU)/mL in FL, and were 10^5.46 and 10^2.64 CFU/mL in CR, respectively. During precipitation, the maximum increase concentrations of R2A, NA culturable bacteria, and coliforms were 10^0.75, 10^1.30, and 10^2.27 CFU/mL in FL, respectively. Furthermore, microbial concentration and rainfall did not increase simultaneously, and a delay phenomenon was observed in the increasing microbial concentrations. Through analyzing the concentration change trends and correlation of various water quality indicators during persistent precipitation, the significant correlation between the DOC concentration and the changes in the dominant species of microbial community structure was found in this study (p < 0.05). For example, as the DOC concentration declined, the abundance of hgcl_clade and CL500-29_marine_group increased. Consequently, although persistent precipitation might not obviously alter the water quality visibly, it could still pose potential microbial risks.

Graphical abstract

Keywords

Rainfall / Dissolved organic carbon / Culturable bacteria / Water quality / Microbial community structure / Climate change

References

[1] Signor R S, Roser D J, Ashbolt N J, Ball J E. (2005). Quantifying the impact of runoff events on microbiological contaminant concentrations entering surface drinking source waters. Journal of Water and Health, 3(4): 453–468

[2] Burgos-Garay M L, Hong C, Moorman G W. (2014). Interactions of heterotrophic bacteria from recycled greenhouse irrigation water with plant pathogenic pythium. HortScience horts, 49(7): 961–967

[3] Burnet J B, Penny C, Ogorzaly L, Cauchie H M. (2014). Spatial and temporal distribution of Cryptosporidium and Giardia in a drinking water resource: implications for monitoring and risk assessment. Science of the Total Environment, 472: 1023–1035

[4] Chen H J, Chang H. (2014). Response of discharge, TSS, and E. coli to rainfall events in urban, suburban, and rural watersheds. Environmental Science. Processes & Impacts, 16(10): 2313–2324

[5] Ciric S, Petrovic O, Milenkovic D. (2010). Low-nutrient R2A medium in monitoring microbiological quality of drinking water. Chemical Industry & Chemical Engineering Quarterly, 16(1): 39–45

[6] Collins R, Elliott S, Adams R. (2005). Overland flow delivery of faecal bacteria to a headwater pastoral stream. Journal of Applied Microbiology, 99(1): 126–132

[7] De Man H, Van Den Berg H H, Leenen E J, Schijven J F, Schets F M, Van Der Vliet J C, Van Knapen F, De Roda Husman A M. (2014). Quantitative assessment of infection risk from exposure to waterborne pathogens in urban floodwater. Water Research, 48: 90–99

[8] Donat M G, Lowry A L, Alexander L V, O’Gorman P A, Maher N. (2016). More extreme precipitation in the world’s dry and wet regions. Nature Climate Change, 6(5): 508–513

[9] Fang W, Lin M, Shi J, Liang Z, Tu X, He Z, Qiu R, Wang S. (2022). Organic carbon and eukaryotic predation synergistically change resistance and resilience of aquatic microbial communities. Science of the Total Environment, 830: 154386

[10] Ferguson C M, Davies C M, Kaucner C, Ashbolt N J, Krogh M, Rodehutskors J, Deere D A. (2007). Field scale quantification of microbial transport from bovine faeces under simulated rainfall events. Journal of Water and Health, 5(1): 83–95

[11] Guo E, Chen L, Sun R, Wang Z. (2015). Effects of riparian vegetation patterns on the distribution and potential loss of soil nutrients: a case study of the Wenyu River in Beijing. Frontiers of Environmental Science & Engineering, 9(2):: 279–287

[12] Guo L, Wan K, Zhu J, Ye C, Chabi K, Yu X. (2021). Detection and distribution of VBNC/viable pathogenic bacteria in full-scale drinking water treatment plants. Journal of Hazardous Materials, 406: 124335

[13] HamersT, Kamstra J H, Van GilsJ, KotteM C, Van Hattum A G (2015). The influence of extreme river discharge conditions on the quality of suspended particulate matter in Rivers Meuse and Rhine (The Netherlands). Environmental Research, 143(Pt A): 241–255

[14] Huang J, Tu Z, Du P, Li Q, Lin J (2012). Analysis of rainfall runoff characteristics from a subtropical urban lawn catchment in South-east China. Frontiers of Environmental Science & Engineering, 6(4): 531–539

[15] Jeng H A C, Englande A J, Bakeer R M, Bradford H B. (2005). Impact of urban stormwater runoff on estuarine environmental quality. Estuarine, Coastal and Shelf Science, 63(4): 513–526

[16] Jeznach L C, Hagemann M, Park M H, Tobiason J E. (2017). Proactive modeling of water quality impacts of extreme precipitation events in a drinking water reservoir. Journal of Environmental Management, 201: 241–251

[17] Kistemann T, Classen T, Koch C, Dangendorf F, Fischeder R, Gebel J, Vacata V, Exner M. (2002). Microbial load of drinking water reservoir tributaries during extreme rainfall and runoff. Applied and Environmental Microbiology, 68(5): 2188–2197

[18] Konapala G, Mishra A K, Wada Y, Mann M E. (2020). Climate change will affect global water availability through compounding changes in seasonal precipitation and evaporation. Nature Communications, 11(1): 3044

[19] Lai H, Hales S, Woodward A, Walker C, Marks E, Pillai A, Chen R X, Morton S M. (2020). Effects of heavy rainfall on waterborne disease hospitalizations among young children in wet and dry areas of New Zealand. Environment International, 145: 106136

[20] Lei H, Yao K, Yang B, Xie L, Ying G (2023).Occurrence, spatial and seasonal variation, and environmental risk of pharmaceutically active compounds in the Pearl River basin, South China. Frontiers of Environmental Science & Engineering, 17(4): 46

[21] Liu X, Liu Z, Zhang Y, Jiang B. (2016). Quantitative analysis of burden of bacillary dysentery associated with floods in Hunan, China. Science of the Total Environment, 547: 190–196

[22] Luo Y, Zhang Y, Lang M, Guo X, Xia T, Wang T, Zhu L (2021). Identification of sources, characteristics and photochemical transformations of dissolved organic matter with EEM-PARAFAC in the Wei River of China. Frontiers of Environmental Science & Engineering, 15, 1–10

[23] Lynch V D, Shaman J. (2022). The effect of seasonal and extreme floods on hospitalizations for Legionnaires’ disease in the United States, 2000–2011. BMC Infectious Diseases, 22(1): 550

[24] Maalej S, Denis M, Dukan S. (2004). Temperature and growth-phase effects on Aeromonas hydrophila survival in natural seawater microcosms: role of protein synthesis and nucleic acid content on viable but temporarily nonculturable response. Microbiology, 150(1): 181–187

[25] Mackowiak M, Leifels M, Hamza I A, Jurzik L, Wingender J. (2018). Distribution of Escherichia coli, coliphages and enteric viruses in water, epilithic biofilms and sediments of an urban river in Germany. Science of the Total Environment, 626: 650–659

[26] Madoux-Humery A S, Dorner S, Sauve S, Aboulfadl K, Galarneau M, Servais P, Prevost M. (2016). The effects of combined sewer overflow events on riverine sources of drinking water. Water Research, 92: 218–227

[27] Mallin M A, Johnson V L, Ensign S H. (2009). Comparative impacts of stormwater runoff on water quality of an urban, a suburban, and a rural stream. Environmental Monitoring and Assessment, 159(1-4): 475–491

[28] Mary P, Sautour M, Chihib N E, Tierny Y, Hornez J P. (2003). Tolerance and starvation induced cross-protection against different stresses in Aeromonas hydrophila. International Journal of Food Microbiology, 87(1-2): 121–130

[29] McCarthy D T, Hathaway J M, Hunt W F, Deletic A. (2012). Intra-event variability of Escherichia coli and total suspended solids in urban stormwater runoff. Water Research, 46(20): 6661–6670

[30] McKergow L A, Davies-Colley R J. (2010). Stormflow dynamics and loads of Escherichia coli in a large mixed land use catchment. Hydrological Processes, 24(3): 276–289

[31] Muirhead R W, Meenken E D. (2018). Variability of Escherichia coli concentrations in rivers during base-flow cconditions in New Zealand. Journal of Environmental Quality, 47(5): 967–973

[32] Paerl H W, Huisman J. (2009). Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports, 1(1): 27–37

[33] Paszko-Kolva C, Yamamoto H, Shahamat M, Sawyer T K, Morris G, Colwell R R. (1991). Isolation of Amoebae and Pseudomonas and Legionella spp. from eyewash stations. Applied and Environmental Microbiology, 57(1): 163–167

[34] Pianetti A, Battistelli M, Citterio B, Parlani C, Falcieri E, Bruscolini F. (2009). Morphological changes of Aeromonas hydrophila in response to osmotic stress. Micron, 40(4): 426–433

[35] Prein A F, Rasmussen R M, Ikeda K, Liu C, Clark M P, Holland G J. (2017). The future intensification of hourly precipitation extremes. Nature Climate Change, 7(1): 48–52

[36] Qiu L, Li Y, Zhong Q, Ma W, Kuang Y, Zhou S, Chen G, Xie J, Hu H, Chen Y. . (2023). Adaptation mechanisms of the soil microbial community under stoichiometric imbalances and nutrient-limiting conditions in a subtropical nitrogen-saturated forest. Plant and Soil, 489(1–2): 239–258

[37] Rechenburg A, Koch C, Classen T, Kistemann T. (2006). Impact of sewage treatment plants and combined sewer overflow basins on the microbiological quality of surface water. Water Science and Technology, 54(3): 95–99

[38] Ruecker A, Uzun H, Karanfil T, Tsui M T K, Chow A T. (2017). Disinfection byproduct precursor dynamics and water treatability during an extreme flooding event in a coastal blackwater river in southeastern United States. Chemosphere, 188: 90–98

[39] Sales-Ortells H, Medema G. (2015). Microbial health risks associated with exposure to stormwater in a water plaza. Water Research, 74: 34–46

[40] Schreiber C, Heinkel S B, Zacharias N, Mertens F M, Christoffels E, Gayer U, Koch C, Kistemann T. (2019). Infectious rain? Evaluation of human pathogen concentrations in stormwater in separate sewer systems. Water Science and Technology, 80(6): 1022–1030

[41] Setty K E, Enault J, Loret J F, Puigdomenech Serra C, Martin-Alonso J, Bartram J. (2018). Time series study of weather, water quality, and acute gastroenteritis at Water Safety Plan implementation sites in France and Spain. International Journal of Hygiene and Environmental Health, 221(4): 714–726

[42] ShaoYXu Y (2023). Challenges and countermeasures of urban water systems against climate change: a perspective from China. Frontiers of Environmental Science & Engineering, 17(12), 156

[43] Tan X, Wu X, Huang Z, Fu J, Tan X, Deng S, Liu Y, Gan T Y, Liu B. (2023). Increasing global precipitation whiplash due to anthropogenic greenhouse gas emissions. Nature Communications, 14(1): 2796

[44] Thackeray C W, Hall A, Norris J, Chen D. (2022). Constraining the increased frequency of global precipitation extremes under warming. Nature Climate Change, 12(5): 441–448

[45] Tornevi A, Bergstedt O, Forsberg B. (2014). Precipitation effects on microbial pollution in a river: lag structures and seasonal effect modification. PLoS One, 9(5): e98546

[46] Wang J, Fan H, He X, Zhang F, Xiao J, Yan Z, Feng J, Li R. (2021). Response of bacterial communities to variation in water quality and physicochemical conditions in a river-reservoir system. Global Ecology and Conservation, 27: e01541

[47] Wortman A T, Bissonnette G K. (1988). Metabolic processes involved in repair of Escherichia coli cells damaged by exposure to acid-mine water. Applied and Environmental Microbiology, 54(8): 1901–1906

[48] Zhang L, Fang W, Li X, Lu W, Li J. (2020a). Strong linkages between dissolved organic matter and the aquatic bacterial community in an urban river. Water Research, 184: 116089

[49] Zhang L, Zhong M, Li X, Lu W, Li J. (2020b). River bacterial community structure and co-occurrence patterns under the influence of different domestic sewage types. Journal of Environmental Management, 266: 110590

[50] Zhang Y, Zou L, Li P, Du Z J, Dou M, Huang Z D, Liang Z J, Qi X B. (2022). Differential characteristics and source contribution of water pollutants before and after the extreme rainfall event in the Huaihe River Basin. Frontiers in Environmental Science, 10: 1003421

[51] Zhong S, Cheng Q, Huang C R, Wang Z. (2021). Establishment and validation of health vulnerability and adaptation indices under extreme weather events on the basis of the 2016 flood in Anhui Province, China. Advances in Climate Change Research, 12(5): 649–659

Acknowledgements

This research was supported by the National Key R&D Program of China (No. 2023YFE0112100), the Natural Science Foundation of China-Joint Fund Project (No. U2005206).

Conflict of Interests

Xin Yu is a response editor of the special issue of Frontiers of Environmental Science & Engineering. The authors declare that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-024-1871-9 and is accessible for authorized users.

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