Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Study of marine bacteria inactivation by photochemical processes: disinfection kinetics and growth modeling after treatment

Abstract

The importance of seawater treatment in order to avoid microbiological pollution related to aquaculture or ballast water management has increased during the last few years. Bacterial indicators used for the evaluation of different disinfection treatments are usually related with both waste and drinking water, these standards are not usual microorganisms found in seawater. Thus, it is thought necessary to study the behavior of different marine-specific organisms in regard to improve the disinfection processes in seawater. In this study, three different bacteria have been selected among major groups of bacterial community from marine waters: two water-associated, Roseobacter sp. and Pseudomonas litoralis, and one sediment-associated, Kocuria rhizophila. A kinetic inactivation model together with a post-treatment growth tendency has been obtained after the application of UV-C and UV/H2O2 processes. According to the first kinetic rate constant, different responses were obtained for the different bacterial groups. Once the treatment was applied, modeling of growth curves revealed high recover within the first 3 days after treatment, even when UV/H2O2 was applied. This study introduces a sensitivity index, in which results show different levels of resistance for both treatments, being Roseobacter sp. the most sensitive bacteria, followed by P. litoralis and K. rhizophila.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Agogué H, Joux F, Obernosterer I, Lebaron P (2005) Resistance of marine bacterioneuston to solar radiation. Appl Environ Microbiol 71(9):5282–5289. https://doi.org/10.1128/AEM.71.9.5282-5289.2005

  2. Aguilar S, Rosado D, Moreno-Andrés J et al (2017) Inactivation of a wild isolated Klebsiella pneumoniae by photo-chemical processes: UV-C, UV-C/H2O2 and UV-C/H2O2/Fe3+. Catal Today 44(5):1334–1338. https://doi.org/10.1016/j.jesp.2008.03.010

  3. Alonso-Sáez L, Gasol JM, Lefort T et al (2006) Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in northwestern Mediterranean coastal waters. Appl Environ Microbiol 72(9):5806–5813. https://doi.org/10.1128/AEM.00597-06

  4. Becerra-Castro C, Macedo G, Silva AMT, Manaia CM, Nunes OC (2016) Proteobacteria become predominant during regrowth after water disinfection. Sci Total Environ 573:313–323. https://doi.org/10.1016/j.scitotenv.2016.08.054

  5. Bolton JR, Linden KG (2003) Standardization of methods for Fluence (UV dose) determination in bench-scale UV experiments. J Environ Eng 129(3):209–215. https://doi.org/10.1061/(ASCE)0733-9372(2003)129:3(209)

  6. Borrero-Santiago AR, Carbú M, DelValls TÁ, Riba I (2016) CO2 leaking from sub-seabed storage: responses of two marine bacteria strains. Mar Environ Res 121:2–8. https://doi.org/10.1016/j.marenvres.2016.05.018

  7. Brinkmeyer R (2016) Diversity of bacteria in ships ballast water as revealed by next generation DNA sequencing. Mar Pollut Bull 107(1):277–285. https://doi.org/10.1016/j.marpolbul.2016.03.058

  8. Buchan A, González JM, Moran MA (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71(10):5665–5677. https://doi.org/10.1128/AEM.71.10.5665

  9. Cerf O (1977) A review tailing of survival curves of bacterial spores. J Appl Bacteriol 42(1):1–19. https://doi.org/10.1111/j.1365-2672.1977.tb00665.x

  10. Cohen AN, Dobbs FC (2015) Failure of the public health testing program for ballast water treatment systems. Mar Pollut Bull 91(1):29–34. https://doi.org/10.1016/j.marpolbul.2014.12.031

  11. Dalrymple OK, Stefanakos E, Trotz MA, Goswami DY (2010) A review of the mechanisms and modeling of photocatalytic disinfection. Appl Catal B Environ 98(1-2):27–38. https://doi.org/10.1016/j.apcatb.2010.05.001

  12. De Schryver P, Vadstein O (2014) Ecological theory as a foundation to control pathogenic invasion in aquaculture. ISME J 8(12):2360–2368. https://doi.org/10.1038/ismej.2014.84

  13. Eisenberg G (1943) Colorimetric determination of hydrogen peroxide. Ind Eng Chem Anal Ed 15(5):327–328. https://doi.org/10.1021/i560117a011

  14. Fujita K, Hagishita T, Kurita S, Kawakura Y, Kobayashi Y, Matsuyama A, Iwahashi H (2006) The cell structural properties of Kocuria rhizophila for aliphatic alcohol exposure. Enzym Microb Technol 39(3):511–518. https://doi.org/10.1016/j.enzmictec.2006.01.033

  15. 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(1):95–105. https://doi.org/10.1016/j.ijfoodmicro.2004.11.038

  16. Giannakis S, Merino Gamo AI, Darakas E, Escalas-Cañellas A, Pulgarin C (2014) Monitoring the post-irradiation E. Coli survival patterns in environmental water matrices: implications in handling solar disinfected wastewater. Chem Eng J 253:366–376. https://doi.org/10.1016/j.cej.2014.05.092

  17. Grob C, Pollet BG (2016) Regrowth in ship’s ballast water tanks: think again! Mar Pollut Bull 109(1):46–48. https://doi.org/10.1016/j.marpolbul.2016.04.061

  18. Hess-Erga O-KK, 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(18):5439–5449. https://doi.org/10.1016/j.watres.2010.06.059

  19. 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(1):3–22. https://doi.org/10.1016/j.watres.2005.10.030

  20. IMO (2004) International convention for the control and management of ships’ ballast water and sediments. BWM/CONF/36

  21. Joint I, Mühling M, Querellou J (2010) Culturing marine bacteria - an essential prerequisite for biodiscovery. Microb Biotechnol 3(5):564–575. https://doi.org/10.1111/j.1751-7915.2010.00188.x

  22. Kim SB, Nedashkovskaya OI, Mikhailov VV et al (2004) Kocuria marina sp. nov., a novel actinobacterium isolated from marine sediment. Int J Syst Evol Microbiol 54(5):1617–1620. https://doi.org/10.1099/ijs.0.02742-0

  23. Leung TY, Chan CY, Hu C, Yu JC, Wong PK (2008) Photocatalytic disinfection of marine bacteria using fluorescent light. Water Res 42(19):4827–4837. https://doi.org/10.1016/j.watres.2008.08.031

  24. Litchman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett 13(12):1560–1572. https://doi.org/10.1111/j.1461-0248.2010.01544.x

  25. Lloyd’s Register (2014) Understanding ballast water management Guidance for shipowners and operators

  26. Lymperopoulou DS, Dobbs FC (2017) Bacterial diversity in ships’ ballast water, ballast-water exchange, and implications for ship-mediated dispersal of microorganisms. Environ Sci Technol 51(4):1962–1972. https://doi.org/10.1021/acs.est.6b03108

  27. Mehrabadi JF, Mirzaie A, Ahangar N, Rahimi A, Rokni-Zadeh H (2016) Draft genome sequence of Kocuria rhizophila RF, a radiation-resistant soil isolate. Genome Announc 4(2):e00095-16. https://doi.org/10.1128/genomeA.00095-16

  28. 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. https://doi.org/10.1016/j.cej.2015.08.079

  29. Moreno-Andrés J, Romero-Martínez L, Acevedo-Merino A, Nebot E (2017) UV-based technologies for marine water disinfection and the application to ballast water: does salinity interfere with disinfection processes? Sci Total Environ 581–582:144–152. https://doi.org/10.1016/j.scitotenv.2016.12.077

  30. Nebot E, Casanueva JF, Casanueva T, Sales D (2007a) Model for fouling deposition on power plant steam condensers cooled with seawater: effect of water velocity and tube material. Int J Heat Mass Transf 50(17-18):3351–3358. https://doi.org/10.1016/j.ijheatmasstransfer.2007.01.022

  31. Nebot E, Salcedo Dávila I, Andrade Balao JAA, Quiroga Alonso JM (2007b) Modelling of reactivation after UV disinfection: effect of UV-C dose on subsequent photoreactivation and dark repair. Water Res 41(14):3141–3151. https://doi.org/10.1016/j.watres.2007.04.008

  32. Nogales B, Aguiló-Ferretjans MM, Martín-Cardona C, Lalucat J, Bosch R (2007) Bacterial diversity, composition and dynamics in and around recreational coastal areas. Environ Microbiol 9(8):1913–1929. https://doi.org/10.1111/j.1462-2920.2007.01308.x

  33. Pascual J, Lucena T, Ruvira MA et al (2012) Pseudomonas Litoralis sp. nov., isolated from mediterranean seawater. Int J Syst Evol Microbiol 62(2):438–444. https://doi.org/10.1099/ijs.0.029447-0

  34. Penru Y, Guastalli AR, Esplugas S, Baig S (2012) Application of UV and UV/H2O2 to seawater: disinfection and natural organic matter removal. J Photochem Photobiol A Chem 233:40–45. https://doi.org/10.1016/j.jphotochem.2012.02.017

  35. Rappé MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57(1):369–394. https://doi.org/10.1146/annurev.micro.57.030502.090759

  36. Romero-Martínez L, Moreno-Andrés J, Acevedo-Merino A, Nebot E (2014) Improvement of ballast water disinfection using a photocatalytic (UV-C + TiO 2 ) flow-through reactor for saltwater treatment. J Chem Technol Biotechnol 89(8):1203–1210. https://doi.org/10.1002/jctb.4385

  37. Rubio D, Nebot E, Casanueva JF, Pulgarin C (2013) 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(16):6367–6379. https://doi.org/10.1016/j.watres.2013.08.006

  38. Rubio D, Casanueva JF, Nebot E (2015) Assessment of the antifouling effect of five different treatment strategies on a seawater cooling system. Appl Therm Eng 85:124–134. https://doi.org/10.1016/j.applthermaleng.2015.03.080

  39. Santos AL, Baptista I, Lopes S, Henriques I, Gomes NCM, Almeida A, Correia A, Cunha  (2012) The UV responses of bacterioneuston and bacterioplankton isolates depend on the physiological condition and involve a metabolic shift. FEMS Microbiol Ecol 80(3):646–658. https://doi.org/10.1111/j.1574-6941.2012.01336.x

  40. Santos AL, Oliveira V, Baptista I, Henriques I, Gomes NCM, Almeida A, Correia A, Cunha  (2013) Wavelength dependence of biological damage induced by UV radiation on bacteria. Arch Microbiol 195(1):63–74. https://doi.org/10.1007/s00203-012-0847-5

  41. Takarada H, Sekine M, Kosugi H, Matsuo Y, Fujisawa T, Omata S, Kishi E, Shimizu A, Tsukatani N, Tanikawa S, Fujita N, Harayama S (2008) Complete genome sequence of the soil actinomycete Kocuria rhizophila. J Bacteriol 190(12):4139–4146. https://doi.org/10.1128/JB.01853-07

  42. Tang JS, Gillevet PM (2003) Reclassification of ATCC 9341 from Micrococcus Luteus to Kocuria rhizophila. Int J Syst Evol Microbiol 53(4):995–997. https://doi.org/10.1099/ijs.0.02372-0

  43. USEPA (2006) Ultraviolet disinfection guidance manual for the final long term 2 enhanced surface water treatment rule. Office of Water (4601), Washington, DC

  44. USEPA (2010) Generic protocol for the verification of ballast water treatment technology

  45. van Rijn J (2013) Waste treatment in recirculating aquaculture systems. Aquac Eng 53:49–56. https://doi.org/10.1016/j.aquaeng.2012.11.010

  46. Vélez-Colmenares JJ, Acevedo A, Nebot E (2011) Effect of recirculation and initial concentration of microorganisms on the disinfection kinetics of Escherichia coli. Desalination 280(1-3):20–26. https://doi.org/10.1016/j.desal.2011.06.041

  47. 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. https://doi.org/10.1016/j.marenvres.2012.10.002

  48. Werschkun B, Banerji S, Basurko OC, David M, Fuhr F, Gollasch S, Grummt T, Haarich M, Jha AN, Kacan S, Kehrer A, Linders J, Mesbahi E, Pughiuc D, Richardson SD, Schwarz-Schulz B, Shah A, Theobald N, von Gunten U, Wieck S, Höfer T (2014) Emerging risks from ballast water treatment: the run-up to the international ballast water management convention. Chemosphere 112:256–266. https://doi.org/10.1016/j.chemosphere.2014.03.135

  49. Widdel F (2010) Theory and measurement of bacterial growth. Grundpraktikum Mikrobiol 4:1–11

  50. Williams PD, Eichstadt SL, Kokjohn TA, Martin EL (2007) Effects of ultraviolet radiation on the gram-positive marine bacterium microbacterium maritypicum. Curr Microbiol 55(1):1–7. https://doi.org/10.1007/s00284-006-0349-2

Download references

Acknowledgements

This research was developed under the R + D Project AVANTE (CTM2014-52116-R) funded by the Spanish Ministry of Economy and Competitiveness.

Author information

Correspondence to Javier Moreno-Andrés.

Additional information

Responsible editor: Vítor Pais Vilar

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Moreno-Andrés, J., Acevedo-Merino, A. & Nebot, E. Study of marine bacteria inactivation by photochemical processes: disinfection kinetics and growth modeling after treatment. Environ Sci Pollut Res 25, 27693–27703 (2018). https://doi.org/10.1007/s11356-017-1185-6

Download citation

Keywords

  • Marine bacteria
  • Ballast water
  • Proteobacteria
  • Actinobacteria
  • UV inactivation
  • Advanced oxidation processes
  • Regrowth