Skip to main content
Log in

Evaluation of ultraviolet disinfection of microalgae by growth modeling: application to ballast water treatment

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Ultraviolet disinfection is a frequent option for eliminating viable organisms in ballast water to fulfill international and national regulations. The objective of this work is to evaluate the reduction of microalgae able to reproduce after UV irradiation, based on their growth features. A monoculture of microalgae Tisochrysis lutea was irradiated with different ultraviolet doses (UV-C 254 nm) by a flow-through reactor. A replicate of each treated sample was held in the dark for 5 days simulating a treatment during the ballasting; another replicate was incubated directly under the light, corresponding to the treatment application during de-ballasting. Periodic measurements of cell density were taken in order to obtain the corresponding growth curves. Irradiated samples depicted a regrowth following a logistic curve in concordance with the applied UV dose. By modeling these curves, it is possible to obtain the initial concentration of organisms able to reproduce for each applied UV dose, thus obtaining the dose-survival profiles, needed to determine the disinfection kinetics. These dose-survival profiles enable detection of a synergic effect between the ultraviolet irradiation and a subsequent dark period; in this sense, the UV dose applied during the ballasting operation and subsequent dark storage exerts a strong influence on microalgae survival. The proposed methodology, based on growth modeling, established a framework for comparing the UV disinfection by different devices and technologies on target organisms. This procedure may also assist the understanding of the evolution of treated organisms in more complex assemblages such as those that exist in natural ballast water.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams JK, Briski E, Ram JL, Bailey SA (2014) Evaluating the response of freshwater organisms to vital staining. Manag Biol Invas 5:197–208

    Article  Google Scholar 

  • Barreto MTO, Melo EP, Almeida JS, Xavier AMRB, Carrondo MJT (1991) A kinetic method for calculating the viability of lactic starter cultures. Appl Microbiol Biotechnol 34:648–652

    Article  Google Scholar 

  • Bendif EM, Probert I, Schroeder DC, de Vargas C (2013) On the description of Tisochrysis lutea gen. nov. sp. nov. and Isochrysis nuda sp. nov. in the Isochrysidales, and the transfer of Dicrateria to the Prymnesiales (Haptophyta). J Appl Phycol 25:1763–1776

    Article  CAS  Google Scholar 

  • Buma AGJ, Vanhannen EJ, Veldhuis MJW, Gieskes WWC (1996) UV-B induces DNA damage and DNA synthesis delay in the marine diatom Cyclotella sp. Sci Mar 60:101–106

    CAS  Google Scholar 

  • Bumbulis MJ, Balog BM (2013) UV-C exposure induces an apoptosis-like process in Euglena gracilis. ISRN Cell Biol 2013:1–6

    Article  Google Scholar 

  • Cerf O, Metro F (1977) Tailing of survival curves of Bacillus licheniformis spores treated with hydrogen peroxide. J Appl Bacteriol 42:405–415

    Article  CAS  PubMed  Google Scholar 

  • Chick H (1908) An investigation of the laws of disinfection. J Hyg (Lond) 8:92–158

    Article  CAS  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Cvetković M, Kompare B, Klemenčič AK (2015) Application of hydrodynamic cavitation in ballast water treatment. Environ Sci Pollut Res 22:7422–7438

    Article  Google Scholar 

  • Drake LA, Doblin MA, Dobbs FC (2007) Potential microbial bioinvasions via ships’ ballast water, sediment, and biofilm. Mar Poll Bull 55:333–341

    Article  CAS  Google Scholar 

  • Ekelund NGA, Danilov RA (2001) The influence of selenium on photosynthesis and “light-enhanced dark respiration” (LEDR) in the flagellate Euglena gracilis after exposure to ultraviolet radiation. Aquat Sci 63:457–465

    Article  CAS  Google Scholar 

  • Eker APM, Hessels JKC, van de Velde J (1988) Photoreactivating enzyme from the green alga Scenedesmus acutus. Evidence for the presence of two different flavin chromophores. Biochemistry 27:1758–1765

    Article  CAS  Google Scholar 

  • Fabregas J, Herrero C, Abalde J, Cabezas B (1985) Growth, chlorophyll a and protein of the marine microalga Isochrysis galbana in batch cultures with different salinities and high nutrient concentrations. Aquaculture 50:1–11

    Article  CAS  Google Scholar 

  • Fafanđel M, Bihari N, Mueller WEG, Batel R (2002) Accumulation and removal of cyclobutane pyrimidine dimers in isochrysis galbana cells exposed to artificial UV and solar irradiation. Period Biol 4:451–456

    Google Scholar 

  • Faimali M, Giussani V, Piazza V, Garaventa F, Corrà C, Asnaghi V, Privitera D, Gallus L, Cattaneo-Vietti R, Mangialajo L, Chiantore M (2012) Toxic effects of harmful benthic dinoflagellate Ostreopsis ovata on invertebrate and vertebrate marine organisms. Mar Environ Res 76:97–107

  • Fan G, Liu D, Lin Q (2013) Fluorescein diacetate and propidium iodide FDA-PI double staining detect the viability of microcystis sp. after ultrasonic irradiation. J Food Agric Environ 11:2419–2421

    Google Scholar 

  • Feng D, Shi J, Sun D (2015) Inactivation of microalgae in ballast water with pulse intense light treatment. Mar Poll Bull 90:299–303

    Article  CAS  Google Scholar 

  • Figawa (2009) Ultraviolet disinfection in water treatment. Technical Report 01 | 08 – Revised Version of Technical Report No. 20/98

  • First MR, Drake LA (2013) Approaches for determining the effects of UV radiation on microorganisms in ballast water. Manag Biol Invas 4:87–99

    Article  Google Scholar 

  • First MR, Drake LA (2014) Life after treatment: detecting living microorganisms following exposure to UV light and chlorine dioxide. J Appl Phycol 26:227–235

    Article  CAS  Google Scholar 

  • First MR, Robbins-Wamsley SH, Riley SC, Drake LA (2016) Towards minimizing transport of aquatic nuisance species in ballast water: Do organisms in different size classes respond uniformly to biocidal treatment? Biol Invas 18:647–660

  • Fisher D, Yonkos L, Ziegler G, Friedel E, Burton D (2014) Acute and chronic toxicity of selected disinfection byproducts to Daphnia magna, Cyprinodon variegatus, and Isochrysis galbana. Water Res 55:233–244

    Article  CAS  PubMed  Google Scholar 

  • Frazier M, Miller AW, Lee H, Reusser DA (2013) Counting at low concentrations: the statistical challenges of verifying ballast water discharge standards. Ecol Appl 23:339–351

    Article  PubMed  Google Scholar 

  • Gallo-Villanueva RC, Jesús-Pérez NM, Martínez-López JI, Pacheco A, Lapizco-Encinas BH (2011) Assessment of microalgae viability employing insulator-based dielectrophoresis. Microfluid Nanofluid 10:1305–1315

    Article  CAS  Google Scholar 

  • Gavand MR, McClintock JB, Amsler CD, Peters RW, Angus RA (2007) Effects of sonication and advanced chemical oxidants on the unicellular green alga Dunaliella tertiolecta and cysts, larvae and adults of the brine shrimp Artemia salina: a prospective treatment to eradicate invasive organisms from ballast water. Mar Poll Bull 54:1777–1788

    Article  CAS  Google Scholar 

  • Geeraerd AH, Herremans CH, Van Impe JF (2000) Structural model requirements to describe microbial inactivation during a mild heat treatment. Int J Food Microbiol 59:185–209

    Article  CAS  PubMed  Google Scholar 

  • Geeraerd AH, Valdramidis VP, Van Impe JF (2005) GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. Int J Food Microbiol 102:95–105

    Article  CAS  PubMed  Google Scholar 

  • Gollasch S, David M, Voigt M, Dragsun E, Hewitt C, Fukuyo Y (2007) Critical review of the IMO international convention on the management of ships’ ballast water and sediments. Harmful Algae 6:585–600

    Article  Google Scholar 

  • Gollasch S, Stehouwer PP, David M (2012) BWO technical outline and requirements for detection systems for establishing compliance enforcement. Final report. Prepared for Interreg IVB North Sea Ballast Water Opportunity project

  • Gollasch S, David M, Francé J, Mozetič P (2015) Quantifying indicatively living phytoplankton cells in ballast water samples—recommendations for Port State Control. Mar Poll Bull 101:768–775

  • Gonsior M, Mitchelmore C, Heyes A, Harir M, Richardson SD, Petty WT, Wright DA, Schmitt-Kopplin P (2015) Bromination of marine dissolved organic matter following full scale electrochemical ballast water disinfection. Environ Sci Technol 49:9048–9055

  • Gorokhova E, Mattsson L, Sundström AM (2012) A comparison of TO-PRO-1 iodide and 5-CFDA-AM staining methods for assessing viability of planktonic algae with epifluorescence microscopy. J Microbiol Methods 89:216–221

    Article  CAS  PubMed  Google Scholar 

  • Hessen D, De Lange H, Van Donk E (1997) UV-induced changes in phytoplankton cells and its effects on grazers. Freshw Biol 38:513–524

    Article  Google Scholar 

  • Hess-Erga OK, Blomvågnes-Bakke B, Vadstein O (2010) Recolonization by heterotrophic bacteria after UV irradiation or ozonation of seawater; a simulation of ballast water treatment. Water Res 44:5439–5449

    Article  CAS  PubMed  Google Scholar 

  • Hijnen WAM, Beerendonk EF, Medema GJ (2006) Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Res 40:3–22

    Article  CAS  PubMed  Google Scholar 

  • Holzinger A, Lütz C (2006) Algae and UV irradiation: effects on ultrastructure and related metabolic functions. Micron 37:190–207

    Article  PubMed  Google Scholar 

  • Jorquera MA, Valencia G, Eguchi M, Katayose M, Riquelme C (2002) Disinfection of seawater for hatchery aquaculture systems using electrolytic water treatment. Aquaculture 207:213–224

    Article  CAS  Google Scholar 

  • Kain J, Fogg G (1958) Studies on the growth of marine phytoplankton. J Mar Biol Ass UK 37:781–788

  • Liebich V, Stehouwer PP, Veldhuis M (2012) Re-growth of potential invasive phytoplankton following UV-based ballast water treatment. Aquat Invas 7:29–36

    Article  Google Scholar 

  • Lloyd’s Register (2015) Understanding ballast water management. Guidance for shipowners and operator. www.lr.org/en/_images/213-35824_Understanding_Ballast_Water_Management_0314_tcm155-248816.pdf. Accessed 24 March 2016

  • Mamlook R, Badran O, Abu-Khader MM, Holdo A, Dales J (2008) Fuzzy sets analysis for ballast water treatment systems: best available control technology. Clean Technol Environ Pol 10:397–407

    Article  Google Scholar 

  • Martínez LF, Mahamud MM, Lavín AG, Bueno JL (2012) Evolution of phytoplankton cultures after ultraviolet light treatment. Mar Poll Bull 64:556–562

    Article  Google Scholar 

  • Martínez LF, Mahamud MM, Lavín AG, Bueno JL (2013) The regrowth of phytoplankton cultures after UV disinfection. Mar Poll Bull 67:152–157

    Article  Google Scholar 

  • Molina E, Sánchez JA, García JL, García F, López D (1992) EPA from Isochrysis galbana. Growth conditions and productivity. Process Biochem 27:299–305

    Article  Google Scholar 

  • Moreno-Andrés J, Romero-Martínez L, Acevedo-Merino A, Nebot E (2016) Determining disinfection efficiency on E. faecalis in saltwater by photolysis of H2O2: implications for ballast water treatment. Chem Eng J 283:1339–1348

    Article  Google Scholar 

  • Oliveri P, Fortunato AE, Petrone L, Ishikawa-Fujiwara T, Kobayashi Y, Todo T, Antonova O, Arboleda E, Zantke J, Tessmar-Raible K, Falciatore A (2014) The cryptochrome/photolyase family in aquatic organisms. Mar Genom 14:23–37

  • Olsen RO, Hess-Erga OK, Larsen A, Ishikawa-Fujiwara T, Kobayashi Y, Todo T, Antonova O, Arboleda E, Zantke J, Tessmar-Raible K, Falciatore A (2015) Flow cytometric applicability to evaluate UV inactivation of phytoplankton in marine water samples. Mar Poll Bull 96:279–285

  • Olsen RO, Hoffmann F, Hess-Erga OK, 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

  • Peleg M, Corradini MG, Normand MD (2007) The logistic (Verhulst) model for sigmoid microbial growth curves revisited. Food Res Int 40:808–818

    Article  Google Scholar 

  • Peperzak L, Brussaard CPD (2011) Flow cytometric applicability of fluorescent vitality probes on phytoplankton. J Phycol 47:692–702

    Article  PubMed  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Poepping C, Beck SE, Wright H, Linden KG (2014) Evaluation of DNA damage reversal during medium-pressure UV disinfection. Water Res 56:181–189

    Article  CAS  PubMed  Google Scholar 

  • Romero-Martínez L, Moreno-Andrés J, Acevedo-Merino A, Nebot E (2014) Improvement of ballast water disinfection using a photocatalytic (UV-C + TiO2) flow-through reactor for saltwater treatment. J Chem Technol Biotechnol 89:1203–1210

    Article  Google Scholar 

  • Rubio D, Casanueva JF, Nebot E (2013a) Improving UV seawater disinfection with immobilized TiO2: study of the viability of photocatalysis (UV254/TiO2) as seawater disinfection technology. J Photochem Photobiol A 271:16–23

    Article  CAS  Google Scholar 

  • Rubio D, Nebot E, Casanueva JF, Pulgarin C (2013b) Comparative effect of simulated solar light, UV, UV/H2O2 and photo-Fenton treatment (UV–vis/H2O2/Fe2+,3+) in the Escherichia coli inactivation in artificial seawater. Water Res 47:6367–6379

    Article  CAS  PubMed  Google Scholar 

  • Ruiz GM, Rawlings TK, Dobbs FC, Drake LA, Mullady T, Huq A, Collwell RR (2000) Global spread of microorganisms by ships. Nature 408:49–50

  • Sahinkaya E, Dilek FB (2009) The growth behavior of Chlorella vulgaris in the presence of 4-chlorophenol and 2,4-dichlorophenol. Ecotoxicol Environ Saf 72:781–786

    Article  CAS  PubMed  Google Scholar 

  • Sakai H, Oguma K, Katayama H, Ohgaki S (2007) Effects of low or medium-pressure UV irradiation on the release of intracellular microcystin. Water Res 41:3458–3464

    Article  CAS  PubMed  Google Scholar 

  • Sanabria J, Wist J, Pulgarin C (2011) Photocatalytic disinfection treatments: viability, cultivability and metabolic changes of E. coli using different measurements methods. Rev Dyna 78:178–187

    Google Scholar 

  • Sánchez S, Martínez ME, Espinola F (2000) Biomass production and biochemical variability of the marine microalga Isochrysis galbana in relation to culture medium. Biochem Eng J 6:13–18

    Article  PubMed  Google Scholar 

  • Sassi J, Rytkönen J, Viitasalo S, Leppäkoski E (2005) Experiments with ultraviolet light, ultrasound and ozone technologies for onboard ballast water treatment. VTT Tied-Valt Tek Tutkimusk 2313:1–80

  • Sato M, Murata Y, Mizusawa M, Iwahashi H, Oka S (2004) A simple and rapid dual-fluorescence viability assay for microalgae. Microbiol Cult Coll 20:53–59

    Google Scholar 

  • Sieracki JL, Bossenbroek JM, Chadderton WL (2014) A spatial modeling approach to predicting the secondary spread of invasive species due to ballast water discharge. PLoS One 9:e114217

  • Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102

    Article  Google Scholar 

  • Smayda TJ (2007) Reflections on the ballast water dispersal-harmful algal bloom paradigm. Harmful Algae 6:601–622

    Article  Google Scholar 

  • Stehouwer PP, Fuhr F, Veldhuis MJW (2010) A novel approach to determine ballast water vitality and viability after treatment. In: Emerging Ballast Water Management Systems; Proceedings of the IMO-WMU Research and Development Forum 26–29 January 2010 Malmö, Sweden. pp 233–240

  • Stehouwer PP, Liebich V, Peperzak L (2013) Flow cytometry, microscopy, and DNA analysis as complementary phytoplankton screening methods in ballast water treatment studies. J Appl Phycol 25:1047–1053

    Article  CAS  Google Scholar 

  • Stehouwer PP, Buma A, Peperzak L (2015) A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide. Environ Technol 36:2094–2104

    Article  CAS  PubMed  Google Scholar 

  • Steinberg MK, Lemieux EJ, Drake LA (2011) Determining the viability of marine protists using a combination of vital, fluorescent stains. Mar Biol 158:1431–1437

    Article  Google Scholar 

  • Steinberg MK, First MR, Lemieux EJ, Drake LA, Nelson BN, Kulis DM, Anderson DM, Welschmeyer NA, Herring PR (2012) Comparison of techniques used to count single-celled viable phytoplankton. J Appl Phycol 24:751–758

  • Sutherland T, Levings C, Elliott C, Hesse W (2001) Effect of ballast water treatment system on survivorship of natural populations of marine plankton. Mar Ecol Prog Ser 210:139–148

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tilney CL, Pokrzywinski KL, Coyne KJ, Warner ME (2014) Growth, death, and photobiology of dinoflagellates (Dinophyceae) under bacterial-algicide control. J Appl Phycol 26:2117–2127

  • USEPA (2006) Ultraviolet disinfection guidance manual for the final long term 2 enhanced surface water treatment rule. EPA 815-R-06-007. U.S. Environmental Protection Agency, Office of Water, Washington, DC

  • van der Star I, Liebich V, Stehouwer PP (2011) The forgotten fraction: the importance of organisms smaller than 10 μm when evaluating ballast water treatment systems. In: Proceedings of the Global R&D Forum on Compliance Monitoring and Enforcement - The next R&D challenge and opportunity. p 41

  • van Slooten C, Wijers T, Buma AGJ, Peperzak L (2015) Development and testing of a rapid, sensitive ATP assay to detect living organisms in ballast water. J Appl Phycol 27:2299–2312

  • Vélez-Colmenares JJ, Acevedo A, Salcedo I, Nebot E (2012) New kinetic model for predicting the photoreactivation of bacteria with sunlight. J Photochem Photobiol B 117:278–285

    Article  PubMed  Google Scholar 

  • Verhulst PF (1838) Notice sur la loi que la population suit dans son accroissement. Corresp Math Phys Publ par A Quetel 10:113–121

    Google Scholar 

  • Viitasalo S, Sassi J (2005) Ozone, ultraviolet light, ultrasound and hydrogen peroxide as ballast water treatments- experiments with mesozooplankton in low-saline brackish water. J Mar Environ Eng 8:35–55

    CAS  Google Scholar 

  • Waite TD, Kazumi J, Lane PVZ, Farmer LL, Smith SG, Smith SL, Hitchcock G, Capo TR (2003) Removal of natural populations of marine plankton by a large-scale ballast water treatment system. Mar Ecol Prog Ser 258:51–63

  • Wennberg AC, Tryland I, Østensvik Ø, Secic I, Monshaugen M, Liltved H (2013) Effect of water treatment on the growth potential of Vibrio cholerae and Vibrio parahaemolyticus in seawater. Mar Environ Res 83:10–15

  • Werschkun B, Sommer Y, Banerji S (2012) Disinfection by-products in ballast water treatment: an evaluation of regulatory data. Water Res 46:4884–4901

    Article  CAS  PubMed  Google Scholar 

  • Wright DA, Welschmeyer NA, Peperzak L (2015) Alternative, indirect measures of ballast water treatment efficacy during a shipboard trial: a case study. J Mar Eng Technol 14:1–8

    Article  Google Scholar 

  • Wu D, You H, Jin D, Li X (2011) Enhanced inactivation of Escherichia coli with Ag-coated TiO2 thin film under UV-C irradiation. J Photochem Photobiol A 217:177–183

    Article  CAS  Google Scholar 

  • Yoshioka M, Yago T, Yoshie-Stark Y, Arakawa H, Morinaga T (2012) Effect of high frequency of intermittent light on the growth and fatty acid profile of Isochrysis galbana. Aquaculture 338–341:111–117

    Article  Google Scholar 

  • Zhang N, Hu K, Shan B (2014) Ballast water treatment using UV/TiO2 advanced oxidation processes: an approach to invasive species prevention. Chem Eng J 243:7–13

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research has been developed under the R+D Project CTM2014-52116-R funded by ERDF of the European Union and FPI Grant BES-2010-029938 by the Spanish Government. Special thanks to Dr. Rosa Vázquez-Gomez and team from the Marine Reserves’ Service of the University of Cadiz for supplying the challenge cultures and advising.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leonardo Romero-Martínez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 252 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romero-Martínez, L., Moreno-Andrés, J., Acevedo-Merino, A. et al. Evaluation of ultraviolet disinfection of microalgae by growth modeling: application to ballast water treatment. J Appl Phycol 28, 2831–2842 (2016). https://doi.org/10.1007/s10811-016-0838-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0838-z

Keywords

Navigation