Abstract
The inactivation of bacteriophage MS2 under irradiation above 320 nm was investigated, focusing on different solution pH, ionic strength, and Suwannee River natural organic matter (SRNOM) concentrations when solutions contained organic or inorganic particle matters. Inorganic and organic particles were modeled using kaolinite (KAO) and Microcystis aeruginosa (MA), respectively. The results showed that the two types of particles influenced on MS2 inactivation under different conditions. The lower pH contributed to the greater MS2 aggregation within pH range of 3.0 to 8.0, leading to an increasing inactivation rate. The presence of KAO induced reactive oxygen species (ROS) under the action of irradiation above 320 nm, which promoted the inactivation of MS2. By comparison, the \(^{1}O_{2}\) produced by MA after irradiation promoted the inactivation at pH < 6, whereas when the pH is ≥ 6, the inactivation effect of MS2 was lower than that of particle-free solution because MS2 was no longer aggregated and MA has a shading effect. In the presence of Na+ or Ca2+ cation, irradiation above 320 nm could not effectively inactivate the MS2 under particle-free solution. By comparison, KAO increased the inactivation efficiency as a photosensitizer. With the increase of Ca2+ concentration, MS2 was more easily adsorbed to MA than aggregation. Until Ca2+ concentration reached 20 mM, the inactivation effect in MA solution was enhanced. In the presence of SRNOM, the inactivation effect increased with the increase of SRNOM concentration. When the SRNOM was 20 mM, the inactivation increased in the particle-free solution due to the greater production of \(^{1}O_{2}\). Compared with the particle-free solution, the KAO and MA inactivation efficiency was lower.
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References
Acra A, Jurdi M, Muallem H (1987) Solar ultraviolet radiation: assessment and application for drinking water disinfection IDRC research results: health sciences division, Collection: 1980s
Abbaszadegan M, Lechevallier MW, Gerba CP (2003) Occurrence of viruses in US groundwaters. J Am Water Works Ass 95(9):107–120. https://doi.org/10.1002/j.1551-8833.2003.tb10458.x
Barbeau B, Huffman D, Mysore C, Desjardins R, Prévost M (2004) Examination of discrete and counfounding effects of water quality parameters during the inactivation of MS2 phages and Bacillus subtilis pores with free chlorine. J Environ Eng Sci 4(3):255–268. https://doi.org/10.1139/s04-002
Beck SE, Rodriguez RA, Hawkins MA, Hargy TM, Larason TC, Linden KG (2016) Comparison of UV-induced inactivation and RNA damage in MS2 phage across the germicidal UV spectrum. Appl Environ Microb 82(5):1468–1474. https://doi.org/10.1128/AEM.02773-15
Bricaud A, Morel A, Prieur L (1981) Absorption by dissolved organic matter of the sea (yellow substance) in the UV and visible domains1. Limnol Oceanogr 26(1):43–53. https://doi.org/10.4319/lo.1981.26.1.0043
Busse MM, Becker M, Applegate BM, Camp JW, Blatchley ER (2019) Responses of Salmonella typhimurium LT2, Vibrio harveyi, and Cryptosporidium parvum to UVB and UVA radiation. Chem Eng J 371:647–656. https://doi.org/10.1016/j.cej.2019.04.105
Canonica S, Jans U, Stemmler K, Hoigne J (1995) Transformation kinetics of phenols in water: photosensitization by dissolved natural organic material and aromatic ketones. Environ Sci Technol 29(7):1822–1831. https://doi.org/10.1021/es00007a020
Chakravarty I, Bhattacharya A, Das SK (2017) Water, sanitation and hygiene: the unfinished agenda in the World Health Organization South-East Asia Region. WHO South-East Asia Journal of Public Health 6(2):22. https://doi.org/10.4103/2224-3151.213787
Chen KL, Elimelech M (2007) Influence of humic acid on the aggregation kinetics of fullerene (C60) nanoparticles in monovalent and divalent electrolyte solutions. J Colloid Interface Sci 309(1):126–134. https://doi.org/10.1016/j.jcis.2007.01.074
Chen H, Lürling M (2020) Calcium promotes formation of large colonies of the cyanobacterium Microcystis by enhancing cell-adhesion. Harmful Algae 92:101768. https://doi.org/10.1016/j.hal.2020.101768
Chen H, Tian W, Ding W (2018) Preparation of meso-Ag/Al2O3 and synergistic water disinfection of metallic silver and ROS under visible light. Sol Energy 173:1065–1072. https://doi.org/10.1016/j.solener.2018.08.047
Daviescolley RJ, Donnison AM, Speed DJ (1997) Sunlight wavelengths inactivating faecal indicator microorganisms in waste stabilisation ponds. Water Sci Technol 35:219–225. https://doi.org/10.2166/wst.1997.0737
Daviscolley RJ, Donnison AM, Speed DJ (2000) Towards a mechanistic understanding of pond disinfection. Water Sci Technol 42:149–158. https://doi.org/10.2166/wst.2000.0630
Degiuseppe JI, Barclay L, Gomes KA, Costantini V, Vinjé J, Stupka JA (2020) Molecular epidemiology of norovirus outbreaks in Argentina, 2013–2018. J Med Virol 92(8):1330–1333. https://doi.org/10.1002/jmv.25684
Dormitzer PR, Sun ZJ, Wagner G, Harrison SC (2002) The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21(5):885–897. https://doi.org/10.1093/emboj/21.5.885
Feng Z, Lu R, Yuan B, Zhou Z, Wu Q, Nguyen TH (2016) Influence of solution chemistry on the inactivation of particle-associated viruses by UV irradiation. Colloids Surf B Biointerfaces 148:622–628. https://doi.org/10.1016/j.colsurfb.2016.09.025
Fisher MB, Iriarte M, Nelson KL (2012) Solar water disinfection (SODIS) of Escherichia coli, Enterococcus spp., and MS2 coliphage: effects of additives and alternative container materials. Water Res 46(6):1745–1754. https://doi.org/10.1016/j.watres.2011.12.048
Fong T, Lipp EK (2005) Enteric viruses of humans and animals in aquatic environments: health risks, detection, and potential water quality assessment tools. Microbiol Mol Biol R 69(2):357–371. https://doi.org/10.1128/MMBR.69.2.357-371.2005
Gerba CP (1984) Applied and theoretical aspects of virus adsorption to surfaces. Adv Appl Microbiol 30:133–168. https://doi.org/10.1016/S0065-2164(08)70054-6
Giannakis S (2018) Analogies and differences among bacterial and viral disinfection by the photo-Fenton process at neutral pH: a mini review. Environ Sci Pollut R 25(28):27676–27692. https://doi.org/10.1007/s11356-017-0926-x
Gutierrez L, Mylon S, Nash B, Nguyen T (2010) Deposition and aggregation kinetics of rotavirus in divalent cation solutions. Environ Sci Technol 44:4552–4557. https://doi.org/10.1021/es100120k
Hamza IA, Jurzik L, Stang A, Sure K, Uberla K, Wilhelm M (2009) Detection of human viruses in rivers of a densly-populated area in Germany using a virus adsorption elution method optimized for PCR analyses. Water Res 43(10):2657–2668. https://doi.org/10.1016/j.watres.2009.03.020
Hu Y, Liu X (2003) Chemical composition and surface property of kaolins. Miner Eng 16(11, Supplement 1):1279–1284. https://doi.org/10.1016/j.mineng.2003.07.006
Huesca-Espitia LLDC, Aurioles-López V, Ramírez I, Sánchez-Salas JL, Bandala ER (2017) Photocatalytic inactivation of highly resistant microorganisms in water: a kinetic approach. J Photochem Photobiol A Chem 337:132–139. https://doi.org/10.1016/j.jphotochem.2017.01.025
Ibarguen-Mondragon E, Revelo-Romo D, Hidalgo A, García H, Galeano L (2020) Mathematical modelling of MS2 virus inactivation by Al/Fe-PILC-activated catalytic wet peroxide oxidation (CWPO). Environ Sci Pollut R 27(16):19836–19844. https://doi.org/10.1007/s11356-020-08365-4
Jacobs A, Lafolie F, Herry JM, Debroux M (2007) Kinetic adhesion of bacterial cells to sand: cell surface properties and adhesion rate. Colloids Surf B Biointerfaces 59(1):35–45. https://doi.org/10.1016/j.colsurfb.2007.04.008
Jermann D, Pronk W, Kägi R, Halbeisen M, Boller M (2008) Influence of interactions between NOM and particles on UF fouling mechanisms. Water Res 42(14):3870–3878. https://doi.org/10.1016/j.watres.2008.05.013
Kirk J (1981) Monte Carlo study of the nature of the underwater light field in, and the relationships between optical properties of, turbid yellow waters. Mar Freshwater Res 32(4):517–532. https://doi.org/10.1071/MF9810517
Kohantorabi M, Giannakis S, Gholami MR, Feng L, Pulgarin C (2019) A systematic investigation on the bactericidal transient species generated by photo-sensitization of natural organic matter (NOM) during solar and photo-Fenton disinfection of surface waters. Appl Catal B 244:983–995. https://doi.org/10.1016/j.apcatb.2018.12.012
Kohn T, Nelson KL (2007) Sunlight-mediated inactivation of MS2 coliphage via exogenous singlet Oxygen produced by sensitizers in natural waters. Environ Sci Technol 41(1):192–197. https://doi.org/10.1021/es061716i
Kohn T, Grandbois M, Mcneill K, Nelson KL (2007) Association with natural organic matter enhances the sunlight-mediated inactivation of MS2 coliphage by singlet oxygen. Environ Sci Technol 41(13):4626–4632. https://doi.org/10.1021/es070295h
Liu Y, Yang C, Li J (2007) Influence of extracellular polymeric substances on pseudomonas aeruginosa transport and deposition profiles in porous media. Environ Sci Technol 41(1):198–205. https://doi.org/10.1021/es061731n
Love DC, Silverman A, Nelson KL (2010) Human virus and bacteriophage inactivation in clear water by simulated sunlight compared to bacteriophage inactivation at a Southern California beach. Environ Sci Technol 44(18):6965–6970. https://doi.org/10.1021/es1001924
Lytle CD, Sagripanti J (2005) Predicted inactivation of viruses of relevance to biodefense by solar radiation. J Virol 79(22):14244–14252. https://doi.org/10.1128/JVI.79.22.14244-14252.2005
Malato S, Fernandezibanez P, Maldonado MI, Blanco J, Gernjak W (2009) Decontamination and disinfection of water by solar photocatalysis: recent overview and trends. Catal Today 147(1):1–59. https://doi.org/10.1016/j.cattod.2009.06.018
Mansoor Ahammed M, Dave S, Nair AT (2014) Effect of water quality parameters on solar water disinfection: a statistical experiment design approach. Desalin Water Treat 56(2):315–326. https://doi.org/10.1080/19443994.2014.940398
Mcminn BR, Ashbolt NJ, Korajkic A (2017) Bacteriophages as indicators of faecal pollution and enteric virus removal. Lett Appl Microbiol 65(1):11–26. https://doi.org/10.1111/lam.12736.6
Miao L, Wang C, Hou J, Wang P, Ao Y, Li Y, Lv B, Yang Y, You G, Xu Y (2016) Effect of alginate on the aggregation kinetics of copper oxide nanoparticles (CuO NPs): bridging interaction and hetero-aggregation induced by Ca2+. Environ Sci Pollut R 23(12):11611–11619. https://doi.org/10.1007/s11356-016-6358-1
Mylon SE, Rinciog CI, Schmidt N, Gutierrez L, Wong G, Nguyen TH (2010) Influence of salts and natural organic matter on the stability of bacteriophage MS2. Langmuir 26(2):1035–1042. https://doi.org/10.1021/la902290t
Nelson KL, Boehm AB, Daviescolley RJ, Dodd MC, Kohn T, Linden KG, Liu Y, Maraccini PA, Mcneill K, Mitch WA (2018) Sunlight-mediated inactivation of health-relevant microorganisms in water: a review of mechanisms and modeling approaches. Environ Sci Process Impacts 20(8):1089–1122. https://doi.org/10.1039/c8em00047f
Nguyen TH, Chen KL (2007) Role of divalent cations in plasmid DNA adsorption to natural organic matter-coated silica surface. Environ Sci Technol 41(15):5370–5375. https://doi.org/10.1021/es070425m
Patel MM, HallVinjé AJJ, Parashar UD (2009) Noroviruses: a comprehensive review. J Clin Virol 44(1):1–8. https://doi.org/10.1016/j.jcv.2008.10.009
Ren M, Drosos M, Frimmel FH (2018) Inhibitory effect of NOM in photocatalysis process: explanation and resolution. Chem Eng J 334:968–975. https://doi.org/10.1016/j.cej.2017.10.099
Rincón A, Pulgarin C (2004) Effect of pH, inorganic ions, organic matter and H2O2 on E. coli K12 photocatalytic inactivation by TiO2: implications in solar water disinfection. Appl Catal B 51(4):283–302. https://doi.org/10.1016/j.apcatb.2004.03.007
Rodgers Michael A. J, Snowden Paul (1982) Lifetime of oxygen (1O2 (1. DELTA. g)) in liquid water as determined by time-resolved infrared luminescence measurements. J Am Chem Soc 104(20):5541–5543. https://doi.org/10.1021/ja00384a070
Romero OC, Straub AP, Kohn T, Nguyen TH (2011) Role of temperature and Suwannee river natural organic matter on inactivation kinetics of rotavirus and bacteriophage MS2 by solar irradiation. Environ Sci Technol 45(24):10385–10393. https://doi.org/10.1021/es202067f
Shan X, Liu L, Li G, Xu K, Liu B, Jiang W (2021) PM2.5 and the typical components cause organelle damage, apoptosis and necrosis: role of reactive oxygen species. Sci Total Environ 782:146785. https://doi.org/10.1016/j.scitotenv.2021.146785
Shishovs M, Rumnieks J, Diebolder CA, Jaudzems K, Andreas LB, Stanek J, Kazaks A, Kotelovica S, Akopjana I, Pintacuda G (2016) Structure of AP205 coat protein reveals circular permutation in ssRNA bacteriophages. J Mol Biol 428(21):4267–4279. https://doi.org/10.1016/j.jmb.2016.08.025
Silverman AI, Nguyen MT, Schilling IE, Wenk J, Nelson KL (2015) Sunlight inactivation of viruses in open-water unit process treatment wetlands: modeling endogenous and exogenous inactivation rates. Environ Sci Technol 49(5):2757–2766. https://doi.org/10.1021/es5049754
Sinton LW, Hall CH, Lynch PA, Daviescolley RJ (2002) Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Appl Environ Microb 68(3):1122–1131. https://doi.org/10.1128/AEM.68.3.1122-1131.2002
Skripkin EA, Adhin MR, De Smit MH, Van Duin J (1990) Secondary structure of the central region of bacteriophage MS2 RNA: conservation and biological significance. J Mol Biol 211(2):447–463. https://doi.org/10.1016/0022-2836(90)90364-R
Song K, Mohseni M, Taghipour F (2019) Mechanisms investigation on bacterial inactivation through combinations of UV wavelengths. Water Res 163:114875. https://doi.org/10.1016/j.watres.2019.114875
Sousa CA, Soares HMVM, Soares EV (2019) Metal(loid) oxide (Al2O3, Mn3O4, SiO2 and SnO2) nanoparticles cause cytotoxicity in yeast via intracellular generation of reactive oxygen species. Appl Microbiol Biot 103(15):6257–6269. https://doi.org/10.1007/s00253-019-09903-y
Squire SA, Ryan U (2017) Cryptosporidium and Giardia in Africa: current and future challenges. Parasit Vector 10(1):195. https://doi.org/10.1186/s13071-017-2111-y
Sun C, Kitajima M, Gin KY (2016) Sunlight inactivation of somatic coliphage in the presence of natural organic matter. Sci Total Environ 541:1–7. https://doi.org/10.1016/j.scitotenv.2015.08.136
Tan X, Zhang D, Duan Z, Parajuli K, Hu J (2020) Effects of light color on interspecific competition between Microcystis aeruginosa and Chlorella pyrenoidosa in batch experiment. Environ Sci Pollut R 27(1):344–352. https://doi.org/10.1007/s11356-019-06650-5
Tang Y, Xin H, Yang S, Guo M, Malkoske T, Yin D, Xia S (2018) Environmental risks of ZnO nanoparticle exposure on Microcystis aeruginosa: toxic effects and environmental feedback. Aquat Toxicol 204:19–26. https://doi.org/10.1016/j.aquatox.2018.08.010
Tang A, Bi X, Li X, Li F, Liao X, Zou J, Sun W, Yuan B (2021) The inactivation of bacteriophage MS2 by sodium hypochlorite in the presence of particles. Chemosphere 266(3):129191. https://doi.org/10.1016/j.chemosphere.2020.129191
Tian Y, Zou J, Feng L, Zhang L, Liu Y (2018) Chlorella vulgaris enhance the photodegradation of chlortetracycline in aqueous solution via extracellular organic matters (EOMs): role of triplet state EOMs. Water Res 149:35–41. https://doi.org/10.1016/j.watres.2018.10.076
Walshe GE, Pang L, Flury M, Close ME, Flintoft M (2010) Effects of pH, ionic strength, dissolved organic matter, and flow rate on the co-transport of MS2 bacteriophages with kaolinite in gravel aquifer media. Water Res 44(4):1255–1269. https://doi.org/10.1016/j.watres.2009.11.034
Wang Y, Araud E, Shisler JL, Nguyen TH, Yuan B (2019) Influence of algal organic matter on MS2 bacteriophage inactivation by ultraviolet irradiation at 220 nm and 254 nm. Chemosphere 214:195–202. https://doi.org/10.1016/j.chemosphere.2018.09.065
Wei L, Li H, Lu J (2021) Algae-induced photodegradation of antibiotics: a review. Environ Pollut 272:115589. https://doi.org/10.1016/j.envpol.2020.115589
Wolff A, Günther T, Albert T, Schilling-Loeffler K, Gadicherla AK, Johne R (2020) Stability of hepatitis E virus at different pH values. Int J Food Microbiol 325:108625. https://doi.org/10.1016/j.ijfoodmicro.2020.108625
Wu X, Feng Z, Yuan B, Zhou Z, Li F, Sun W (2018) Effects of solution chemistry on the sunlight inactivation of particles-associated viruses MS2. Colloids Surf B Biointerfaces 162:179–185. https://doi.org/10.1016/j.colsurfb.2017.11.056
Yuan B, Pham M, Nguyen TH (2008) Deposition kinetics of bacteriophage MS2 on a silica surface coated with natural organic matter in a radial stagnation point flow cell. Environ Sci Technol 42(20):7628–7633. https://doi.org/10.1021/es801003s
Zhang W, Zhang X (2015) Adsorption of MS2 on oxide nanoparticles affects chlorine disinfection and solar inactivation. Water Res 69:59–67. https://doi.org/10.1016/j.watres.2014.11.013
Acknowledgements
The authors greatly appreciated the financial support from the Natural Science Foundation of China (Grant No. 51678255, 51178117), the Science and Technology Major Project of the Bureau of Science and Technology of Xiamen (Grant No. 3502Z20191012), and the Quanzhou City Sciences & Technology Program of China (Grant No. 2018C082R).
Funding
The Natural Science Foundation of China (Grant No. 51678255, 51178117), Science and Technology Major Project of the Bureau of Science and Technology of Xiamen (Grant No. 3502Z20191012), and Quanzhou City Sciences & Technology Program of China (Grant No. 2018C082R).
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Xiaoxue Li: writing — original draft, visualization, formal analysis; Xiaochao Bi: writing — review & editing; Xiaoyang Shi: conceptualization, investigation; Rao La: validation; Ming-Lai Fu, Wenjie Sun: validation, writing — review & editing; Baoling Yuan: resources, supervision.
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Highlights
• The interaction between MS2 and particles under irradiation above 320 nm was studied.
• \({1}_{{O}_{2}}\) produced by MS2 capsid protein under irradiation promoted inactivation at low pH.
• High concentration of Ca2+ enhanced the inactivation in the solution with particles.
• The increased of SRNOM enhanced the inactivation whether were particles free or not.
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Li, X., Bi, X., Shi, X. et al. Effect of particulate matters on inactivation of bacteriophage MS2 under irradiation above 320 nm. Environ Sci Pollut Res 29, 73976–73986 (2022). https://doi.org/10.1007/s11356-022-20811-z
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DOI: https://doi.org/10.1007/s11356-022-20811-z