Abstract
The aim of this study was to evaluate the effects of short-term (hours) exposure to solar UV radiation (UVR, 280–400 nm) on the physiology of Microcystis aeruginosa. Three solar radiation treatments were implemented: (i) PAR (PAR, 400–700 nm), (ii) TUVA (PAR + UVAR, 315–700 nm) and (iii) TUVR (PAR + UVAR + UVBR, 280–700 nm). Differential responses of antioxidant enzymes and the reactive oxygen species (ROS) production to UVR were observed. Antioxidant enzymes were more active at high UVR doses. However, different responses were observed depending on the exposure to UVAR or UVBR and the dose level. No effects were observed on the biomass, ROS production or increased activity of superoxide dismutase (SOD) and catalase (CAT) compared to the control when UVR + PAR doses were lower than 9875 kJ m−2. For intermediate doses, UVR + PAR doses between 9875 and 10 275 kJ m−2, oxidative stress increased while resistance was imparted through SOD and CAT in the cells exposed to UVAR. Despite the increased antioxidant activity, biomass decrease and photosynthesis inhibition were observed, but no effects were observed with added exposure to UVBR. At the highest doses (UVR + PAR higher than 10 275 kJ m−2), the solar UVR caused decreased photosynthesis and biomass with only activation of CAT by UVBR and SOD and CAT by UVAR. In addition, for such doses, a significant decrease of microcystins (MCs, measured as MC-LR equivalents) was observed as a consequence of UVAR. This study facilitates our understanding of the SOD and CAT protection according to UVAR and UVBR doses and cellular damage and reinforces the importance of UVR as an environmental stressor. In addition, our results support the hypothesized antioxidant function of MCs.
References
G. Pérez, S. Doldán, O. Borsani and P. Irisarri, Differential Response to Moderate UV-B Irradiation of Two Heterocystous Cyanobacteria Isolated from a Temperate Ricefield, Adv. Microbiol., 2012, 2(01), 37.
J. B. Kerr and C. T. McElroy, Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion, Science, 1993, 262(5136), 1032.
S. Solomon, D. J. Ivy, D. Kinnison, M. J. Mills, R. R. Neely and A. Schmidt, Emergence of healing in the Antarctic ozone layer, Science, 2016, 353, 269–274.
I. Chorus and J. Bartram, Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management, World Health Organization/E&FN Spon/ Routledge, London, 1999.
R. L. Oliver and G. G. Ganf, Freshwater blooms, in The ecology of cyanobacteria, Springer, Netherlands, 2000, pp. 149–194.
F. Garcia-Pichel, Solar ultraviolet and the evolutionary history of cyanobacteria, Orig. Life Evol. Biosph., 1998, 28(3), 321.
R. P. Rastogi, S. P. Singh, A. Incharoensakdi, D. P. Häder and R. P. Sinha, Ultraviolet radiation-induced generation of reactive oxygen species, DNA damage and induction of UV- absorbing compounds in the cyanobacterium Rivularia sp. HKAR-4, S. Afr.J. Bot., 2014, 90, 163.
Y. Y. He and D. P. Häder, UV-B-induced formation of reactive oxygen species and oxidative damage of the cyano- bacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-L-cysteine, J. Photochem. Photobiol., B, 2002, 66(2), 115.
Y. Y. He and D. P. Häder, Involvement of reactive oxygen species in the UV-B damage to the cyanobacterium Anabaena sp, J. Photochem. Photobiol., B, 2002, 66(1), 73.
A. Hargreaves, F. A. Taiwo, O. Duggan, S. H. Kirk and S. I. Ahmad, Near-ultraviolet photolysis of β-phenylpyruvic acid generates free radicals and results in DNA damage, J. Photochem. Photobiol., B, 2007, 89(2), 110.
I. Vass, E. Turcsányi, E. Touloupakis, D. Ghanotakis and V. Petrouleas, The mechanism of UV-A radiation-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence, Biochemistry, 2002, 41(32), 10200.
A. Latifi, M. Ruiz and C. C. Zhang, Oxidative stress in cyanobacteria, FEMS Microbiol. Rev., 2009, 33(2), 258.
M. Blumthaler and A. R. Webb, UVR climatology, in UV effects in aquatic organisms and ecosystems. Comprehensive Series in Photochemical and Photobiological Sciences, ed. E. W. Helbling and H. E. Zagarese, The Royal Society of Chemistry, Cambridge, 2003, pp. 21–58.
M. P. Hernando, G. F. Malanga and G. A. Ferreyra, Oxidative stress and antioxidant defences generated by solar UV in a Subantarctic marine phytoflagellate, Sci. Mar., 2005, 69(S2), 287.
M. Hernando, I. Schloss, S. Roy and G. Ferreyra, Photoacclimation to Long-Term Ultraviolet Radiation Exposure of Natural Sub-Antarctic Phytoplankton Communities: Fixed Surface Incubations Versus Mixed Mesocosms, Photochem. Photobiol., 2006, 82(4), 923.
M. Ehling Schulz and S. Scherer, UV protection in cyano- bacteria, Eur. J. Phycol., 1999, 34(4), 329.
J. A. Imlay, Pathways of oxidative damage, Annu. Rev. Microbiol., 2003, 57(1), 395.
A. A. Gorman and M. A. Rodgers, Current perspectives of singlet oxygen detection in biological environments, J. Photochem. Photobiol., B, 1992, 14(3), 159.
H. Qian, S. Yu, Z. Sun, X. Xie, W. Liu and Z. Fu, Effects of copper sulfate, hydrogen peroxide and N-phenyl-2-naphthyl- amine on oxidative stress and the expression of genes involved photosynthesis and microcystin disposition in Microcystis aeruginosa, Aquat. Toxicol., 2010, 99(3), 405.
G. C. Dismukes, V. V. Klimov, S. V. Baranov, Y. N. Kozlov, J. DasGupta and A. Tyryshkin, The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosyn- thesis, Proc. Natl. Acad. Sci. U. S. A., 2001, 98(5), 2170.
M. Hernando, C. Houghton, L. Giannuzzi, B. Krock, D. Andrinolo and G. Malanga, Oxidative stress in Microcystis aeruginosa as a consequence of global climate change, Biocell, 2016, 40(1), 23.
P. T. Orr and G. J. Jones, Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures, Limnol. Oceanogr., 1998, 43(7), 1604.
R. Kurmayer, E. Dittmann, J. Fastner and I. Chorus, Diversity of microcystin genes within a population of the toxic cyanobacterium Microcystis spp. in lake Wannsee (Berlin, Germany), Microb. Ecol., 2002, 43(1), 107.
B. Sedmak and T. Eleršek, Microcystins induce morpho- logical and physiological changes in selected representative phytoplanktons, Microb. Ecol., 2005, 50(2), 298.
M. Yoshida, T. Yoshida, Y. Takashima, N. Hosoda and S. Hiroishi, Dynamics of microcystin-producing and non- microcystin-producing Microcystis populations is corre- lated with nitrate concentration in a Japanese lake, FEMS Microbiol. Lett., 2007, 266(1), 49.
A. M. Hotto, M. F. Satchwell, D. L. Berry, C. J. Gobler and G. L. Boyer, Spatial and temporal diversity of microcystins and microcystin-producing genotypes in Oneida Lake, NY, Harmful Algae, 2008, 7(5), 671.
C. Dziallas and H. P. Grossart, Increasing oxygen radicals and water temperature select for toxic Microcystis sp, PLoS One, 2011, 6(9), 25569.
L. Giannuzzi, B. Krock, M. C. CrettazMinaglia, L. Rosso, C. Houghton, D. Sedan, G. Malanga, M. Espinosa, D. Andrinolo and M. Hernando, Growth, toxin production, active oxygen species and catalase activity of Microcystis aeru- ginosa (Cyanophyceae) exposed to temperature stress, Comp. Biochem Physiol., Part C: Toxicol. Pharmacol., 2016, 189, 22.
L. Rosso, D. Sedan, M. Kolman, J. Caixach, C. Flores, J. M. Oteiza, G. Salerno, R. Echenique, L. Giannuzzi and D. Andrinolo, Microcystisaeruginos strain [D-Leu1] Mcyst- LR producer, from Buenos Aires province, Argentina, J. Coastal Life Med., 2014, 2(4), 287.
R. Rippka, J. Deruelles, J. B. Waterbury, M. Herdman and R. Y. Stanier, Generic assignments, strain histories and pro- perties of pure cultures of cyanobacteria, Microbiology, 1979, 111(1), 1.
M. P. Hernando and G. A. Ferreyra, The effects of UV radi- ation on photosynthesis in an Antarctic diatom (Thalassiosira sp.): Does vertical mixing matter?, J. Exp. Mar. Biol. Ecol., 2005, 325(1), 35.
S. Diaz, C. Camilion, G. Deferrari, H. Fuenzalida, R. Armstrong, C. Booth, A. Paladini, S. Cabrera, C. Casiccia, C. Lovengreen, J. Pedroni, A. Rosales, H. Zagarese and M. Vernet, Ozone and UV radiation over southern South America: climatology and anomalies, Photochem. Photobiol., 2006, 82, 834.
L. V. Orce and E. W. Helbling, Latitudinal UVR/PAR measurements in Argentina: extent of the “ozone hole”, Glob. Planet. Change, 1997, 15, 113.
O. Holm Hansen, C. J. Lorenzen, R. W. Holmes and J. D. Strickland, Fluorometric determination of chlorophyll, ICES J. Mar. Sci., 1965, 30(1), 3–15.
S. T. Jeffrey and G. F. Humphrey, New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton, Biochem. Physiol. Pflanz., 1975, 167(2), 191.
V. E. Villafañe and F. M. H. Reid, Métodos de microscopía para la cuantificación del fitoplancton, in Manual de métodos ficológicos, Universidad de Concepción, Concepción, 1995, p. 169.
R. E. McDowell, C. D. Amsler, D. A. Dickinson, J. B. McClintock and B. J. Baker, Reactive oxygen species and the Antarctic macroalgal wound response, J. Phycol., 2014, 50(1), 71.
B. Halliwell and J. M. Gutteridge, Free Radicals in Biology and Medicine, Oxford University Press, New York, 2007.
E. Beutler, Catalase, in Red Cell Metabolism a Manual Of Biochemical Methods, ed. E. Beutler, Grune and Stratton, Inc, 1982, p. 105.
N. Steeman, The use or radiocarbon (14C) for measuring organic production in the sea, J. Cons. Int. Explor. Mer., 1952, 18, 117–140.
S. M. Scheiner, Multiple response variables and multi- species interactions, in Design and analysis of ecological experiments, ed. S. M. Scheiner and J. Gurevitch, Chapman & Hall, New York, 2nd edn, 2001, p. 99.
S. P. Singh, D. P. Häder and R. P. Sinha, Cyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategies, Ageing Res. Rev., 2010, 9(2), 79.
V. P. Singh, P. K. Srivastava and S. M. Prasad, Differential effects of UV-B radiation fluence rates on growth, photosyn- thesis, and phosphate metabolism in two cyanobacteria under copper toxicity, Toxicol. Environ. Chem., 2012, 94(8), 1511.
D. P. Häder, H. D. Kumar, R. C. Smith and R. C. Worrest, Effects of solar UV radiation on aquatic ecosystems and interactions with climate change, Photochem. Photobiol. Sci., 2007, 6, 267.
Y. Ding, L. Song and B. Sedmak, UVB radiation as a poten- tial selective factor favoring microcystin producing bloom forming cyanobacteria, PLoS One, 2013, 8(9), 73919.
N. Blot, D. Mella Flores, C. Six, G. Le Corguillé, C. Boutte, A. Peyrat and L. Garczarek, Light history influences the response of the marine cyanobacterium Synechococcus sp. WH7803 to oxidative stress, Plant Physiol., 2011, 156(4), 1934.
A. L. Dany, T. Douki, C. Triantaphylides and J. Cadet, Repairof the main UV-induced thymine dimeric lesions within Arabidopsis thaliana DNA: evidence for the major involvement of photoreactivation pathways, J. Photochem. Photobiol., B, 2001, 65, 127.
H. W. Paerl, J. Tucker and P. T. Bland, Carotenoid enhance- mentand its role in maintaining blue-green algae (Microcystis aeruginosa) surface blooms, Limnol. Oceanogr., 1983, 28, 847.
Z. Yang and F. Kong, UV-B Exposure affects the biosynthesis of microcystin in toxic Microcystis aeruginosa cells and its degradation in the extracellular space, Toxins, 2015, 7, 4238.
A. Canini, D. Leonardi and M. G. Caiola, Superoxide dis- mutase activity in the cyanobacterium Microcystis aerugi- nosa after surface bloom formation, New Phytol., 2001, 152(1), 107.
R. P. Sinha and D. P. Häder, UV-induced DNA damage and repair: a review, Photochem. Photobiol. Sci., 2002, 1(4), 225.
N. Kaul and H. J. Forman, Reactive oxygen species in physiology and toxicology: from lipid peroxidation to transcriptional activation, Toxicol. Hum. Environ.: The Critical Role of Free Radicals, 2000, 311.
P. Chelikani, I. Fita and P. C. Loewen, Diversity of struc- tures and properties among catalases, Cell. Mol. Life Sci., 2004, 61(2), 192.
C. T. Nomura, T. Sakamoto and D. A. Bryant, Roles for heme-copper oxidases in extreme high-light and oxidative stress response in the cyanobacterium Synechococcus sp. PCC 7002, Arch. Microbiol., 2006, 185(6), 471.
R. W. Castenholz and F. Garcia Pichel, Cyanobacterial responses to UV-radiation, in The ecology of cyanobacteria, Springer, Netherlands, 2000, p. 591.
H. Frohnmeyer and D. Staiger, Ultraviolet-B radiation- mediated responses in plants. Balancing damage and pro- tection, Plant Physiol., 2003, 133(4), 1420.
B. A. Brown and G. I. Jenkins, UV-B signaling pathways with different fluence-rate response profiles are distin- guished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH, Plant Physiol., 2008, 146(2), 576.
Y. N. Feng, Z. C. Zhang, J. L. Feng and B. S. Qiu, Effects of UV-B radiation and periodic desiccation on the morpho- genesis of the edible terrestrial cyanobacterium Nostoc fla- gelliforme, Appl. Environ. Microbiol., 2012, 78(19), 7075.
J. E. Frederick, H. F. Snell and E. K. Haywood, Solar ultra- violet radiation at the earth’s surface, Photochem. Photobiol., 1989, 50, 443.
B. L. Montgomery, Sensing the light: photoreceptive systems and signal transduction in cyanobacteria, Mol. Microbiol., 2007, 64(1), 16.
B. Demmig-Adams and W. W. Adams Iii, Photoprotection and other responses of plants to high light stress, Annu. Rev. Plant Biol., 1992, 43(1), 599.
E. M. Aro, I. Virgin and B. Andersson, Photoinhibition of photosystem II. Inactivation, protein damage and turnover, Biochim. Biophys. Acta, Bioenerg., 1993, 1143(2), 113–134.
C. I. Sicora, S. E. Appleton, C. M. Brown, J. Chung, J. Chandler, A. M. Cockshutt, I. Vass and D. A. Campbell, Cyanobacterial psbA families in Anabaena and Synechocystis encode trace, constitutive and UVB-induced D1 isoforms, Biochim. Biophys. Acta, Bioenerg., 2006, 1757(1), 47.
Y. Nishiyama, S. I. Allakhverdiev, H. Yamamoto, H. Hayashi and N. Murata, Singlet oxygen inhibits the repair of photo- system II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803, Biochemistry, 2004, 43(35), 11321.
M. M. Caldwell, J. F. Bornman, C. L. Ballaré, S. D. Flint and G. Kulandaivelu, Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors, Photochem. Photobiol. Sci., 2007, 6(3), 252.
Y. Zilliges, J. C. Kehr, S. Meissner, K. Ishida, S. Mikkat, M. Hagemann, A. Kaplan, T. Börner and E. Dittmann, The cyanobacterial hepatotoxinmicrocystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions, PLoS One, 2011, 6(3), 17615.
M. Kaebernick, B. Neilan, T. Börner and E. Dittmann, Light and the Transcriptional Response of the Microcystin Biosynthesis Gene Cluster, Appl. Environ. Microbiol., 2000, 66(8), 3387.
S. Meissner, D. Steinhauser and E. Dittmann, Metabolomic analysis indicates a pivotal role of the hepatotoxin micro- cystin in high light adaptation of Microcystis, Environ. Microbiol., 2015, 17, 1497.
A. K. Makower, J. M. Schuurmans, D. Groth, Y. Zilliges, H. C. P. Matthijs and E. Dittmann, Transcriptomics-Aided Dissection of the Intracellular and Extracellular Roles of Microcystin in Microcystis aeruginosa PCC 7806, Appl. Environ. Microbiol., 2015, 81, 544.
E. Briand, C. Yéprémian, J. F. Humbert and C. Quiblier, Competition between microcystin- and non-microcystin- producing Planktothrix agardhii (cyanobacteria) strains under different environmental conditions, Environ. Microbiol., 2008, 10, 3337.
R. Sommaruga, Y. Chen and Z. Liu, Multiple Strategies of Bloom-Forming Microcystis to Minimize Damage by Solar Ultraviolet Radiation in Surface Waters, Microb. Ecol., 2009, 57, 667.
H. Jiang and B. Qiu, Photosynthetic adaptation of a bloom forming cyanobacterium Microcystis aeruginosa to prolonged UV-B exposure, J. Phycol., 2005, 41, 983.
Acknowledgments
This study was supported by grants from the University of Buenos Aires, ANPCyT and CONICET. We are thankful to Dr S. Díaz who shared the Biospherical Inc. radiometer and Dr. Opezzo-Costa and her group for laboratory support. We would especially like to thank the personnel from Universidad de Chilecito for fieldwork and laboratory support. We thank two anonymous reviewers who, with their comments and suggestions, helped us to improve this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hernando, M., Minaglia, M.C.C., Malanga, G. et al. Physiological responses and toxin production of Microcystis aeruginosa in short-term exposure to solar UV radiation. Photochem Photobiol Sci 17, 69–80 (2018). https://doi.org/10.1039/c7pp00265c
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1039/c7pp00265c