Abstract
This study describes the ability of a yeast strain, Aureobasidium pullulans KKUY0701 isolated from eutrophic lake to eliminate Cylindrospermopsis raciborskii and cylindrospermopsin (CYN) toxin. The anti-cyanobacterial activity of this yeast strain was evaluated by growing with living cells and filtrate of C. raciborskii. CYN bioremoval was assayed using living and heat-inactivated yeast cells. Both living cells and filtrate of this yeast strain were able to suppress the growth of C. raciborskii, with total cell death occurring at day 2 and day 3, respectively. Living and inactivated yeast cells, but not yeast filtrate, reduced CYN concentrations released into cyanobacterial cultures, indicating that this toxin might be removed from the culture medium via absorption onto yeast surface rather than enzymatic biodegradation. The adsorption experiments also confirmed the elimination of CYN by living and heat-inactivated yeast. Nevertheless, inactivated yeast exhibited higher capacity (K = 3.3) and intensity (n = 1.4) than living yeast (K = 1.9, n = 1) for CYN adsorption. The study suggests that this yeast strain could be employed for bioremediation of Cylindrospermopsis blooms in freshwaters. Additionally, heat-inactivated yeast biomass could be used in slow sand filters for elimination of CYN in drinking water treatment plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable
References
Baptista AS, Horii J, Calori-Domingues MA, da Gloria EM, Salgado JM, Vizioli MR (2004) The capacity of manno-oligosaccharides, thermolysed yeast and active yeast to attenuate aflatoxicosis. World J Microbiol Biotechnol 20:475–481. https://doi.org/10.1023/B:WIBI.0000040397.48873.3b
Bazin E, Mourot A, Humpage AR, Fessard V (2010) Genotoxicity of a freshwater cyanotoxin, cylindrospermopsin, in two human cell lines: Caco-2 and HepaRG. Environ Mol Mutagen 51:251–259. https://doi.org/10.1002/em.20539
Burford MA, Davis TW (2011) Physical and chemical processes promoting dominance of the toxic cyanobacterium Cylindrospermopsis raciborskii. Chin J Oceanol Limnol 29:883–891. https://doi.org/10.1007/s00343-011-0517-5
Burford MA, Beardall J, Willis A, Orr PY, Magalhaes VF, Rangel LM, Azevedo SMFOE, Neilan BA (2016) Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae 54:44–53
Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203:264–272. https://doi.org/10.1016/j.taap.2004.02.016
Di Francesco A, Roberti R, Martini C, Baraldi E, Mari M (2015) Activities of Aureobasidium pullulans cell filtrates against Monilinia laxa of peaches. Microbiol Res 181:61–67. https://doi.org/10.1016/j.micres.2015.09.003
Di Francesco A, Ugolini L, D’Aquino S, Pagnotta E, Mari M (2017) Biocontrol of Monilinia laxa by Aureobasidium pullulans strains: insights on competition for nutrients and space. Int J Food Microbiol 248:32–38. https://doi.org/10.1016/j.ijfoodmicro.2017.02.007
Han G, Feng X, Jia Y, Wang C, He X, Zhou Q, Tian X (2011) Isolation and evaluation of terrestrial fungi with algicidal ability from Zijin Mountain, Nanjing. China J Microbiol 49(348):562–567. https://doi.org/10.1007/s12275-011-0496-4
Hou X, Huang J, Tang WNA, Zhang LU, Gu L (2019) Allelopathic inhibition of juglone (5-hydroxy-1,4-naphthoquinone) on the growth and physiological performance in Microcystis aeruginosa. J Environ Manage 232:382–386. https://doi.org/10.1016/j.jenvman.2018.11.105
Jia Y, Han G, Wang C, Guo P, Jiang W, LiX Tian X (2010) The efficacy and mechanisms of fungal suppression of freshwater harmful algal bloom species. J Hazard Mater 183:176-363 181 364. https://doi.org/10.1016/j.jhazmat.2010.07.009
Jia Y, Han GM, Wang CY, Guo P, Jiang WX, Li XN, Tian XJ (2010b) The efficacy and mechanisms of fungal suppression of freshwater harmful algal bloom species. J Hazard Mat 183:176–181. https://doi.org/10.1016/j.jhazmat.2010.07.009
Jia Y, Wang Q, Chen ZH, Jiang WX, Zhang P, Tian XJ (2010c) Inhibition of phytoplankton species by co-culture with a fungus. Ecol Eng 36:1389–1391. https://doi.org/10.1016/j.ecoleng.2010.06.017
Jia Y, Wang C, Zhao G, Guo P, Tian X (2012a) The possibility of using cyanobacterial bloom materials as a medium for white rot fungi. Lett Appl Microbiol 54(96–101):366. https://doi.org/10.1111/j.1472-765X.2011.03178.x
Jia Y, Jingjing DU, Song F, Zhao G, Tian X (2012b) A fungus capable of degrading microcystin-LR in the algal culture of Microcystis aeruginosa PCC7806. Appl Biochem Biotechnol 166:987–996. https://doi.org/10.1007/s12010-011-9486-6
Kurtzman CP, Fell JF (1998) The yeasts, a taxonomic study. Elsevier, Amsterdam, pp 77–101
Lee C, Jeon MS, Thi-Thao T, Park C, Jong-Soon Choi J, Kwon J, Roh SW, Yoon-E Choi YE (2018) Establishment of a new strategy against Microcystis bloom using newlyisolated lytic and toxin-degrading bacteria. J Appl Phycol 30:1795–1806. https://doi.org/10.1007/s10811-018-1403-8
Lei L, Dai J, Lin Q, Peng L (2020) Competitive dominance of Microcystis aeruginosa against Raphidiopsis raciborskii is strain and temperature-dependent. Know1 Manag Aquat Ecosyst 421:36. https://doi.org/10.1051/kmae/2020023
Li N, Zhang L, Li F, Wang Y, Zhu Y, Kang H (2011) Metagenome of microorganisms associated with the toxic cyanobacteria Microcystis aeruginosa analyzed using the sequencing platform. Chinese J Oceanol Limnol 29:505–513. https://doi.org/10.1007/s00343-011-0056-0
Liu Y (2017). Treatment of the cyanotoxins cylindrospermopsin, microcystin-LR, and anatoxin-a by activated carbon in drinking water. UW Space. http://hdl.handle.net/ 10012/12178
Luo Y, Wang J, Liu B, Wang Z, Yuan Y, Yue T (2015) Effect of yeast cell morphology, cell wall physical structure and chemical composition on patulin adsorption. PLoS One 10:e0136045. https://doi.org/10.1371/journal.pone.0136045
Massey IY, Yang F (2020) A mini review on microcystins and bacteria degradation. Toxins 12:268. https://doi.org/10.3390/toxins12040268
Mohamed ZA, AlShehri AM (2007) Cyanobacteria and their toxins in treated-water storage reservoirs in Abha city, Saudi Arabia. Toxicon 50:75–78. https://doi.org/10.1016/j.toxicon.2007.02.021
Mohamed ZA, AlShehri AM (2010) Differential responses of epiphytic and planktonic toxic cyanobacteria to allelopathic substances of the submerged macrophyte Stratiotes aloides. Int Rev Hydrobiol 95(3):224–234. https://doi.org/10.1002/iroh.200911219
Mohamed ZA, Al-Shehri AM (2013) Assessment of cylindrospermopsin toxin in an arid Saudi lake containing dense cyanobacterial bloom. Environ Monitor Assess 185:2157–2166. https://doi.org/10.1007/s10661-012-2696-8
Mohamed ZA, Hashem M, Alamri SA (2014) Growth inhibition of the cyanobacterium Microcystis aeruginosa and degradation of its microcystin toxins by the fungus Trichoderma citrinoviride. Toxicon 86:51–58. https://doi.org/10.1016/j.toxicon.2014.05.008
Mohamed ZA, Deyab MA, Abou-Dobara MI, Kamel A, El-Raghi WM (2015) Occurrence of cyanobacteria and microcystin toxins in raw and treated waters of the Nile River, Egypt: implication for water treatment and human health. Environ Sci Poll Res 22:11716–11727. https://doi.org/10.1007/s11356-015-4420-z
Mohamed ZA, Alamri S, Hashem M, Mostafa Y (2020) Growth inhibition of Microcystis aeruginosa and adsorption of microcystin toxin by the yeast Aureobasidium pullulans, with no effect on microalgae. Environ Sci Pollut Res Int 395(27):38038–38046. https://doi.org/10.1007/s11356-020-09902-x
Möllers KB, Cannella D, Jørgensen H, Frigaard N-U (2014) Cyanobacterial biomass as carbohydrate and nutrient feedstock for bioethanol production by yeast fermentation. Biotechnol Biofuel 7:64. https://doi.org/10.1186/1754-6834-7-64
Ndlela LL, Oberholster PJ, Van Wyk JH, Cheng PH (2018) Bacteria as biological control agents of freshwater cyanobacteria: is it feasible beyond the laboratory? Appl Microbiol Biotechnol 102:9911–9923. https://doi.org/10.1007/s00253-018-9391-9
Nishu SD, Kang Y, Han I, Jung TY, Lee TK (2019) Nutritional status regulates algicidal activity of Aeromonas sp. L23 against cyanobacteria and green algae. PLoS ONE 14(3):e0213370. https://doi.org/10.1371/journal.pone.0213370
Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65(102):9911–9923. https://doi.org/10.1007/s00248-012-0159-y
Petruzzi L, Corbo MR, Baiano A, Beneduce L, Sinigaglia M, Bevilacqua A (2015) In vivo stability of the complex OchratoxinA – Saccharomyces cerevisiae starter strains. Food Control 50:516–520. https://doi.org/10.1016/j.foodcont.2014.09.042
Prasongsuk S, Lotrakul P, Ali I, Bankeeree W, Punnapayak H (2018) The current status of Aureobasidium pullulans in biotechnology. Folia Microbiol 63:129–140. https://doi.org/10.1007/s12223-017-0561-4
Shao J, Li R, Lepo JE, Gu J-D (2013) Potential for control of harmful cyanobacterial blooms using biologically derived substances: problems and prospects. J Environ Manage 125:149–155. https://doi.org/10.1016/j.jenvman.2013.04.001
Svircev Z, Obradovic V, Codd GA, Marjanovic P, Spoof L, Drobac D (2016) Massive fish mortality and Cylindrospermopsis raciborskii bloom in Aleksandrovac Lake. Ecotoxicol 25:1353–1363. https://doi.org/10.1007/s10646-016-1687-x
Thomson K, Bhat A, Carvell J (2015) Comparison of a new digital imaging technique for yeast cell counting and viability assessments with traditional methods. J Instit Brew 121:231–237
Van Apeldoorn ME, van Egmond HP, Speijers GJA, Bakker GJI (2007) Toxins of cyanobacteria. Mol Nutr Food Res 51:7–60. https://doi.org/10.1016/j.hal.2007.07.004
Van Wichelen J, Vanormelingen P, Codd GA, Vyverman W (2016) The common bloom-forming cyanobacterium Microcystis is prone to a wide array of microbial antagonists. Harmful Algae 55:97–111. https://doi.org/10.1016/j.hal.2016.02.009
Vero S, Mondino P, Burgueno J, Soubes M, Wisniewski M (2002) Characterization of biocontrol activity of two yeast strains from Uruguay against blue mold of apple. Postharv Biol Technol 26:91–98. https://doi.org/10.1016/S0925-5214(01)00199-5
Weiss G, Kovalerchick D, Lieman-Hurwitz J, Murik O, De Philippis R, Carmeli S, Sukenik A, Kaplan A (2019) Increased algicidal activity of Aeromonas veronii in response to Microcystis aeruginosa: interspecies crosstalk and secondary metabolites synergism. Environ Microbiol 21:1140–1150. https://doi.org/10.1111/14622920.14561
WHO (2020). Cyanobacterial toxins: cylindrospermopsin. Background document for development of WHO Guidelines for drinking-water quality and Guidelines for safe recreational water environments. World Health Organization, Geneva, Switzerland (WHO/HEP/ECH/ WSH/2020.4)
Wilkens SL, Maas EW (2012) Development of a novel technique for axenic isolation and culture of Thraustochytrids from New Zealand marine environments. J Appl Microbiol 112:346–352. https://doi.org/10.1111/j.13652672.2011.05197.x
Wormer L, Cires A, Carrasco D, Quesada A (2008) Cylindrospermopsin is not degraded by co-occurring natural bacterial communities during a 40-day study. Harmful Algae 7:206–213. https://doi.org/10.1016/j.hal.2007.07.004
Acknowledgements
The authors extend their appreciation to the Deanship of Scientific Research, King Khalid University for funding this work through research groups program under grant number R.G.P. 1/97/43.
Funding
The authors declare that funding received from Deanship of Scientific Research, King Khalid University for funding this work through research groups program under grant number R.G.P. 1/97/43 was used in the design experiments and collection, statistical analysis, data interpretation, and writing the manuscript.
Author information
Authors and Affiliations
Contributions
MH, SA, and YM cultured A. pullulans strain and followed its growth in bioremoval experiments. ZM collected and tabulated data of anti-cyanobacterial and toxin-degrading yeast. ZM set up the experiments of anti-cyanobacterial activity of A. pullulans and cylindrospermopsin adsorption and was a major contributor in writing the manuscript. All authors participated in analysis and interpretation of the data and read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Vitor Vasconcelos.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mohamed, Z., Alamri, S., Hashem, M. et al. Bioremoval of Cylindrospermopsis raciborskii cells and cylindrospermopsin toxin in batch culture by the yeast Aureobasidium pullulans. Environ Sci Pollut Res 29, 90140–90146 (2022). https://doi.org/10.1007/s11356-022-22069-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-22069-x