Abstract
Microalgae pose major problems for drinking water treatment processes either through membrane fouling or through blooming events in source water during the summer months. Disinfection treatments such as chlorination and UV-C treatment of drinking water are designed to remove microorganisms including microalgae and bacteria. In order to treat water efficiently it is critical to understand the effect of UV-C treatment on the viability and vitality of phytoplankton. Moreover, this information can be used to assess the utility of UV-C treatment as a potential pre-treatment option for water clean-up. In this study we tested the population growth of 6 phytoplankton species representing three major taxonomic groups (green algae, diatoms and cyanobacteria), commonly found in freshwater lakes in North America and relevant for water treatment facilities. We exposed these species to UV-C treatment and monitored their post-exposure population growth over a 52–55-day period using a plate-based MPN (most probable number) method. We found the green alga Scenedesmus quadricauda and the cyanobacterium Anabaena flos-aquae to be most tolerant to the treatment, while the cyanobacterium Microcystis aeruginosa and the diatom Asterionella formosa were found to be most sensitive with viability being reduced at comparatively lower doses. No significant delays in growth post treatment (i.e. time lags) were reported within species. Asterionella formosa and Aulacoseira granulata showed the longest time lags of all species, which might be in part correlated with DNA repair mechanisms and other physiological adaptations. This work provides the basis for the assessment of UV-C treatment efficacy on freshwater phytoplankton.
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References
Adhikary SP, Sahu JK (1998) UV protecting pigment of the terrestrial cyanobacterium Tolypothrix byssoidea. J Plant Physiol 153:770–773
Aguirre LE, Ouyang L, Elfwing A, Hedblom M, Wulff A, Inganäs O (2018) Diatom frustules protect DNA from ultraviolet light. Sci Rep 8:5138
Ahmed F, Fanning K, Netzel M, Schenk PM (2015) Induced carotenoid accumulation in Dunaliella salina and Tetraselmis suecica by plant hormones and UV-C radiation. Appl Microbiol Biotechnol 99:9407–9416
Alam ZB, Otaki M, Furumai H, Ohgaki S (2001) Direct and indirect activation of Microcystis aeruginosa by UV-radiation. Water Res 35:1008–1014
Barasanti L, Gualtieri P (2014) Algae: anatomy, biochemistry and biotechnology, 2nd edn. CRC Press, Boca Raton
Betancourt WQ, Rose JB (2004) Drinking water treatment processes for removal of Cryptosporidium and Giardia. Vet Parasitol 126:219–234
Blatchley ER, Cullen J, Petri B, Bircher K, Welschmeyer N (2018) The biological basis for ballast water performance standards: “viable/non-viable” or “live/dead”. Environ Sci Technol 52:8075–8086
Borderie F, Alaoui-Sehmer L, Bousta F, Alaoui-Sossé B, Aleya L (2014) Cellular and molecular damage caused by high UV-C irradiation of the cave-harvested green alga Chlorella minutissima: implications for cave management. Int Biodeterior Biodegrad 93:118–130
Casas-Monroy O, Linley RD, Chan P, Kydd J, Byllaardt JV, Bailey S (2017) Evaluating efficacy of filtration + UV-C radiation for ballast water treatment at different temperatures. J Sea Res 133:20–28
Chiou Y, Hsieh M, Yeh H (2010) Effect of algal extracellular polymer substances on UF membrane fouling. Desalination 250:648–652
Cooper JT, Kannan MS, Kalleyer DE (2011) Bacillariophyta: the diatoms. In: American Water Works Association (ed) Algae: source to treatment. American Water Works Association, Denver, pp 207–246
Cullen JJ (2018) Quantitative framework for validating two methodologies that enumerate viable organisms or type approval of ballast water management systems. Sci Total Environ 627:1602–1626
Cullen JJ, MacIntyre HL (2016) On the use of the serial dilution culture method to enumerate viable phytoplankton in natural communities of plankton subjected to ballast water treatment. J Appl Phycol 28:279–298
De Stefano L, De Stefano M, Maddalena P, Moretti L, Rea I, Mocella V, Rendina I (2007) Playing with light in diatoms: small water organisms with a natural photonic crystal structure. Proc SPIE 659313
Deng L, Wenshan G, Ngo HH, Zhang H, Wang J, Li J, Xia S, Wi Y (2016) Biofouling and control approaches in membrane bioreactors. Bioresour Technol 221:656–665
Dionisio-Sese M (2010) Aquatic microalgae as potential sources of UV-screening compounds. Philipp J Sci 139:5–16
Ellegaard M, Lenau T, Lundholm N, Maibohm C, Friis SMM, Rottwitt K, Si Y (2016) The fascinating diatom frustule- can it play a role for attenuation of UV radiation. J Appl Phycol 28:3295–3306
Estepp LR, Reavie ED (2015) The ecological history of Lake Ontario according to phytoplankton. J Great Lakes Res 41:669–687
Falconer IR, Humpage AR (2005) Health risk assessment of cyanobacterial (blue-green algal) toxins in drinking water. Int J Environ Res Public Health 2:43–50
Gao Y, Cui Y, Xiong W, Li X, Wi Q (2009) Effect of UV-C on algal evolution and differences in growth rate, pigmentation and photosynthesis between prokaryotic and eukaryotic algae. Photochem Photobiol 85:774–782
Gao W, Liang H, Ma J, Chen Z, Han Z, Li G (2011) Membrane fouling control in ultrafiltration technology for drinking water production: A review. Desalination 272:1–8
Hannach G, Sigleo AC (1998) Photoinduction of UV-absorbing compounds in six species of marine phytoplankton. Mar Ecol Prog Ser 174:207–222
Health Canada (2006) It’s your health: drinking water chlorination. Government of Canada. https://www.canada.ca/en/health-canada/services/healthy-living/your-health/environment/drinking-water-chlorination.html. Accessed 16 February 2020
Health Canada (2019) Guidelines for Canadian drinking water quality guideline technical document; enteric viruses. Government of Canada. https://www.canada.ca/en/health-canada/services/publications/healthy-living/guidelines-canadian-drinking-water-quality-guideline-technical-document-enteric-viruses.html. Accessed 17 July 2020
Holzinger A, Lütz C (2006) Algae and UV irradiation: effects on ultrastructure and related metabolic functions. Micron 37:190–207
Hull NM, Isola MR, Petri B, Chan P, Linden KG (2017) Algal DNA repair kinetics support culture-based enumeration for validation of ultraviolet disinfection ballast water treatment systems. Environ Sci Technol Lett 4:192–196
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta Bioenerg 1817:182–193
Jimoh TA, Cowan AK (2017) Extracellular polymeric substance production in high rate algal oxidation ponds. Water Sci Technol 76:2647–2654
Karentz D, Cleaver JE, Mitchell DL (1991) Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation. J Phycol 27:326–341
Kim J, Chung Y, Shin D, Kim M, Lee Y, Lim Y, Lee D (2002) Chlorination by-products in surface water treatment process. Desalination 151:1–9
King WD, Marrett LD (1996) Case-control study of bladder cancer and chlorination by-products in treated water (Ontario, Canada). Cancer Causes Control 7:596–604
Knappe DRU, Belk RC, Briley DS, Gandy SR, Rastogi N, Rike AH, Glasgow H, Hannon E, Frazier WD, Kohl P, Pugsley S (2004) Algae detection and removal strategies for drinking water treatment plants. American Water Works Association and AWWA Research Foundation, Denver
Kuhlman KR, Allenbach LB, Ball CL, Fusco WG, La Duc MT, Kuhlman GM, Anderson RC, Stuecker T, Erickson IK, Benardini J, Crawford RL (2005) Enumeration, isolation, and characterization of ultraviolet (UV-C) resistant bacteria from rock varnish in the Whipple Mountains, California. Icarus 174:585–595
Kumar D, Keshari N, Suku P, Adhikary SP (2019) Response of the sub-aerial cyanobacterium Scytonema millei to UV-C irradiation. Indian J Exp Biol 57:362–367
Leynaert A, Fardel C, Beker B, Soler C, Delebecq G, Lemercier A, Pondaven P, Durand PE, Heggarty K (2018) Diatom frustule nanostructure in pelagic and benthic environments. Silicon 10:2701–2709
Liebich V, Stehouwer PP, Veldhuis M (2012) Re-growth of potential invasive phytoplankton following UV-based ballast water treatment. Aquat Invasions 7:29–36
Lundgreen K, Holbech H, Pedersen KL, Petersen GI, Andreasen RR, George C, Drillet G, Andersen M (2018) UV Fluences required for compliance with ballast water discharge standards using two approved methods for algal viability assessment. Mar Pollut Bull 135:1090–1100
Ma Z, Gao K (2010) Spiral breakage and photoinhibition of Arthrospira platensis (Cyanophyta) caused by accumulation of reactive oxygen species under solar radiation. Environ Exp Bot 68:208–213
MacIntyre HL, Cullen JJ (2005) Using cultures to investigate the physiological ecology of microalgae. In: Andersen RA (ed) Algal culture techniques. Academic Press, New York, pp 287–326
MacIntyre HL, Cullen JJ (2016) Classification of phytoplankton cells as live or dead using the vital stains fluorescein diacetate and 5‐chloromethylfluorescein diacetate. J Phycol 52:572–589
MacIntyre HL, Cullen JJ, Whitsitt TJ, Petri B (2018) Enumerating viable phytoplankton using a culture-based Most Probable Number assay following ultraviolet-C treatment. J Appl Phycol 30:1073–1094
MacKenzie AF, Maltby EA, Harper N, Bueley C, Olender D, Wyeth RC (2019) Periodic ultraviolet-C illumination for marine sensor antifouling. Biofouling 35:483–493
Martin RB, Markus DDR, Sutherland TF (2018) The effect of ultraviolet light (UV-C) on marine phytoplankton fluorescence. Can Tech Rep Fish Aquat Sci 3289:1–18
Martínez LF, Mahamud MM, Lavín AG, Bueno JL (2013) The regrowth of phytoplankton cultures after UV disinfection. Mar Pollut Bull 67:152–157
Masojídek J, Kopecká J, Koblížek M, Torzillo G (2004) The xanthophyll cycle in green algae (Chlorophyta): Its role in the photosynthetic apparatus. Plant Biol 6:342–349
Michalak AM, Anderson EJ, Beletsky D, Boland S, Bosch NS, Bridgeman TB, Chaffin JD, Cho K, Confesor R, Daloglu I, DePinto JV, Evans MA, Fahnenstiel GL, He L, Ho JC, Jenkins L, Johengen TH, Kuo KC, LaPorte E, Liu X, McWilliams MR, Moore MR, Posselt DJ, Richards RP, Scavia D, Steiner AL, Verhamme E, Wright DM, Zagorski MA (2013) Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proc Natl Acad Sci 110:6448–6452
Micheik A, Cassaignon S, Livage J, Gibaud A, Berthier S, Lopez PJ (2018) Optical properties of nanostructured silica structures from marine organisms. Front Mar Sci 5:123
Munawar M, Munawar IF (1986) The seasonality of phytoplanktonin North American Great Lakes, a comparative synthesis. Hydrobiologia 138:85–115
National Research Council (US) Safe Drinking Water Committee (1980) Drinking water and health: volume 2. National Academies Press (US). Accessed 12 February 2020
Nguyen T, Roddick FA, Fan L (2012) Biofouling of water treatment membranes: a review of the underlying causes, monitoring techniques and control measures. Membranes 2:804–840
Nichols HW (1979) Growth media – freshwater. In: Stein JR (ed) Handbook of phycological methods, culture methods & growth measurements. Cambridge University Press, Cambridge, pp 8–20
Niyogi KK, Björkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci 94:14162–14167
Olsen RO, Hoffmann F, Hess-Erga O, Larsen A, Thuestad G, Hoell IA (2016) Ultraviolet radiation as a ballast water treatment strategy: inactivation of phytoplankton measured with flow cytometry. Mar Pollut Bull 103:270–275
Ou H, Gao N, Deng Y, Wang H, Zhang H (2011) Inactivation and degradation of Microcystis aeruginosa by UV-C irradiation. Chemosphere 85:1192–1198
Ou H, Gao N, Deng Y, Qiao J, Wang H (2012) Intermediate and long term impacts of UV-C irradiation on photosynthetic capacity, survival and microcystin-LR release risk of Microcystis aeruginosa. Water Res 46:1241–1250
Palmer CM (1962) Algae in water supplies of Ohio. OJS 62:225–244
Palmer CM (1977) Algae and water pollution: An illustrated manual on the identification, significance, and control of algae in water supplies and in polluted water (EPA/600/9-77/036). Office of Research and Development, US Environmental Protection Agency. https://nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=20013HX0.TXT. Accessed 11 February 2019
Patnaik J, Swain N, Adhikary SP (1993) Differential response of two species of the cyanobacterium Anabaena to ultraviolet (UV-C) irradiation. J Basic Microbiol 33:427–432
Proteau PJ, Gerwick WH, Garcia-Pichel F, Castenholz R (1993) The structure of scytonemin, an ultraviolet sunscreen pigment from the sheaths of cyanobacteria. Experentia 49:825–829
Rastogi RP, Richa KA, Tyagi MB, Sinha RP (2010) Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic Acids 2010:592980
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Sakai H, Oguma K, Katayama H, Ohgaki S (2007) Effects of low- or medium-pressure ultraviolet lamp irradiation on Microcystis aeruginosa and Anabaena variabilis. Water Res 41:11–18
Sakai H, Katayama H, Oguma K, Ohgaki S (2011) Effect of photoreactivation on ultraviolet inactivation of Microcystis aeruginosa. Water Sci Technol 63:1224–1229
Sathasivam R, Ki J (2018) A review of the biological activities of microalgal carotenoids and their potential use in healthcare and cosmetic industries. Mar Drugs 16:26
Singh SP, Hӓder D, Sinha RP (2010) Cyanobacteria and ultraviolet radiation (UVR) stress: Mitigation strategies. Ageing Res Rev 9:79–90
Sinha RP, Hӓder D (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236
Song K, Mohseni M, Taghipour F (2019) Mechanisms investigation on bacterial inactivation through combinations of UV wavelengths. Water Res 163:114875
Stal LJ, Henley WJ, Kvíderová J, Kirkwood AE, Milner J, Potter AT (2007) Cyanobacteria: diversity and versality, clues to life in extreme environments. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Dordrecht, pp 661–675
Statistics Canada (2013) Survey of drinking water plants 2011. Ministry of Industry. https://www150.statcan.gc.ca/n1/en/pub/16-403-x/16-403-×2013001-eng.pdf?st=US8MT0YO. Accessed 21 April 2020
Su Y, Lenau TA, Gundersen E, Kirkensgaard JJK, Maibohm C, Pinti J, Ellegaard M (2018) The UV filtering potential of drop-casted layers of frustule of three diatom species. Sci Rep 8:959
Sutherland TF, Levings CD, Elliott CC, Hesse WW (2001) Effect of a ballast water treatment system on survivorship of natural populations of marine plankton. Mar Ecol Prog Ser 210:139–148
Svrcek C, Smith DW (2004) Cyanobacteria toxins and the current state of knowledge on water treatment options: a review. J Environ Eng Sci 3:155–185
Takaichi S (2011) Carotenoids in algae: distribution, biosynthesis and function. Mar Drugs 9:1101–1118
Tao Y, Zhang X, Au DWT, Mao X, Yuan K (2010) The effects of sub-lethal UV-C irradiation on growth and cell integrity of cyanobacteria and green algae. Chemosphere 78:541–547
Tao Y, Mao X, Hu J, Mok HOL, Wang L, Au DWT, Zhu J, Zhang X (2013) Mechanisms of photosynthetic inactivation on growth suppression of Microcystis aeruginosa under UV-C stress. Chemosphere 93:637–644
Throndsen J (1978) The dilution-culture method. In: Sournia A (ed) Phytoplankton manual. UNESCO, Paris, pp 218–224
Trojan UV Resources (2018) UV vs. chlorine for wastewater disinfection. https://www.resources.trojanuv.com/uv-vs-chlorine-water-disinfection/. Accessed 11 February 2019
United States Environmental Protection Agency [USEPA] (2006) Ultraviolet Disinfection Guidance Manual for the Final Long Term 2 Enhanced Surface Water Treatment Rule. Office of Water, Washington
Wells ML, Trainer VL, Smayda TJ, Karlson BSO, Trick CG, Kudela RM, Ishikawa A, Bernard S, Wulff A, Anderson DM, Cochlan WP (2015) Harmful algal blooms and climate change: learning from the past and present to forecast the future. Harmful Algae 49:68–93
Xiong F, Komenda J, Kopecký J, Nedbal L (1997) Strategies of ultraviolet-B protection in microscopic algae. Physiol Plant 100:378–388
Zyara AM, Torvinen E, Veijalainen A, Heinonen-Tanski H (2016) The effect of UV and combined chlorine/UV treatment on coliphages in drinking water disinfection. Water 8:130
Acknowledgements
We would like to start by thanking the University of Guelph and the Department of Integrative Biology for the space and materials to conduct the research. We would like to acknowledge Trojan Technologies Ltd. for allowing us to use their UV equipment. We would also like to thank Dr. Josef Ackerman and Dr. Paul Sibley for their feedback and support during this project. We would also like to thank Dr. George Harauz and Dr. Vladimir Bamm for the use of the POLARstar Omega microplate reader to monitor microalgal growth.
Funding
The research in this study was funded by NSERC CRD grants to Andreas Heyland (Grant numbers [501331] and [053535]).
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JR and AH designed and executed the experiments, performed the analysis and wrote the manuscript. Feedback on experimental design and data analysis was provided by PSC, BP and TM. KN assisted with algal cultures and monitoring of experiments.
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Research presented in this manuscript was in part funded by Trojan Technologies through an NSERC CRD project grant.
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Roszell, J., Chan, PS., Petri, B. et al. Divergent responses of diverse microalgae commonly found in drinking water source water to UV-C treatment. J Appl Phycol 33, 1541–1557 (2021). https://doi.org/10.1007/s10811-021-02404-4
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DOI: https://doi.org/10.1007/s10811-021-02404-4