Skip to main content
SpringerLink
Log in

Physiological responses and toxin production of Microcystis aeruginosa in short-term exposure to solar UV radiation

  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. 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.

    Article  CAS  Google Scholar 

  2. 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.

    Article  CAS  PubMed  Google Scholar 

  3. 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.

    Article  CAS  PubMed  Google Scholar 

  4. 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.

    Book  Google Scholar 

  5. R. L. Oliver and G. G. Ganf, Freshwater blooms, in The ecology of cyanobacteria, Springer, Netherlands, 2000, pp. 149–194.

    Google Scholar 

  6. F. Garcia-Pichel, Solar ultraviolet and the evolutionary history of cyanobacteria, Orig. Life Evol. Biosph., 1998, 28(3), 321.

    Article  CAS  PubMed  Google Scholar 

  7. 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.

    Article  CAS  Google Scholar 

  8. 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.

    Article  CAS  Google Scholar 

  9. 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.

    Article  CAS  Google Scholar 

  10. 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.

    Article  CAS  Google Scholar 

  11. 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.

    Article  CAS  PubMed  Google Scholar 

  12. A. Latifi, M. Ruiz and C. C. Zhang, Oxidative stress in cyanobacteria, FEMS Microbiol. Rev., 2009, 33(2), 258.

    Article  CAS  PubMed  Google Scholar 

  13. 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.

    Google Scholar 

  14. 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.

    Article  CAS  Google Scholar 

  15. 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.

    Article  CAS  PubMed  Google Scholar 

  16. M. Ehling Schulz and S. Scherer, UV protection in cyano- bacteria, Eur. J. Phycol., 1999, 34(4), 329.

    Article  Google Scholar 

  17. J. A. Imlay, Pathways of oxidative damage, Annu. Rev. Microbiol., 2003, 57(1), 395.

    Article  CAS  PubMed  Google Scholar 

  18. A. A. Gorman and M. A. Rodgers, Current perspectives of singlet oxygen detection in biological environments, J. Photochem. Photobiol., B, 1992, 14(3), 159.

    Article  CAS  Google Scholar 

  19. 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.

    Article  CAS  PubMed  Google Scholar 

  20. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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.

    Article  CAS  Google Scholar 

  22. 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.

    Article  CAS  Google Scholar 

  23. 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.

    Article  CAS  PubMed  Google Scholar 

  24. B. Sedmak and T. Eleršek, Microcystins induce morpho- logical and physiological changes in selected representative phytoplanktons, Microb. Ecol., 2005, 50(2), 298.

    Article  CAS  PubMed  Google Scholar 

  25. 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.

    Article  CAS  PubMed  Google Scholar 

  26. 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.

    Article  CAS  Google Scholar 

  27. C. Dziallas and H. P. Grossart, Increasing oxygen radicals and water temperature select for toxic Microcystis sp, PLoS One, 2011, 6(9), 25569.

    Article  CAS  Google Scholar 

  28. 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.

    CAS  Google Scholar 

  29. 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.

    CAS  Google Scholar 

  30. 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.

    Article  Google Scholar 

  31. 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.

    Article  CAS  Google Scholar 

  32. 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.

    Article  CAS  PubMed  Google Scholar 

  33. L. V. Orce and E. W. Helbling, Latitudinal UVR/PAR measurements in Argentina: extent of the “ozone hole”, Glob. Planet. Change, 1997, 15, 113.

    Article  Google Scholar 

  34. 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.

    Article  CAS  Google Scholar 

  35. 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.

    Article  CAS  Google Scholar 

  36. 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.

    Google Scholar 

  37. 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.

    Article  CAS  PubMed  Google Scholar 

  38. B. Halliwell and J. M. Gutteridge, Free Radicals in Biology and Medicine, Oxford University Press, New York, 2007.

    Google Scholar 

  39. E. Beutler, Catalase, in Red Cell Metabolism a Manual Of Biochemical Methods, ed. E. Beutler, Grune and Stratton, Inc, 1982, p. 105.

    Google Scholar 

  40. N. Steeman, The use or radiocarbon (14C) for measuring organic production in the sea, J. Cons. Int. Explor. Mer., 1952, 18, 117–140.

    Article  Google Scholar 

  41. 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.

    Google Scholar 

  42. 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.

    Article  CAS  PubMed  Google Scholar 

  43. 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.

    Article  CAS  Google Scholar 

  44. 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.

    Article  PubMed  Google Scholar 

  45. 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.

    Article  CAS  Google Scholar 

  46. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. 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.

    Article  CAS  Google Scholar 

  48. 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.

    Article  CAS  Google Scholar 

  49. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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.

    Article  CAS  Google Scholar 

  51. R. P. Sinha and D. P. Häder, UV-induced DNA damage and repair: a review, Photochem. Photobiol. Sci., 2002, 1(4), 225.

    Article  CAS  PubMed  Google Scholar 

  52. 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.

    Google Scholar 

  53. P. Chelikani, I. Fita and P. C. Loewen, Diversity of struc- tures and properties among catalases, Cell. Mol. Life Sci., 2004, 61(2), 192.

    Article  CAS  PubMed  Google Scholar 

  54. 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.

    Article  CAS  PubMed  Google Scholar 

  55. R. W. Castenholz and F. Garcia Pichel, Cyanobacterial responses to UV-radiation, in The ecology of cyanobacteria, Springer, Netherlands, 2000, p. 591.

    Google Scholar 

  56. H. Frohnmeyer and D. Staiger, Ultraviolet-B radiation- mediated responses in plants. Balancing damage and pro- tection, Plant Physiol., 2003, 133(4), 1420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. J. E. Frederick, H. F. Snell and E. K. Haywood, Solar ultra- violet radiation at the earth’s surface, Photochem. Photobiol., 1989, 50, 443.

    Article  CAS  Google Scholar 

  60. B. L. Montgomery, Sensing the light: photoreceptive systems and signal transduction in cyanobacteria, Mol. Microbiol., 2007, 64(1), 16.

    Article  CAS  PubMed  Google Scholar 

  61. 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.

    Article  CAS  Google Scholar 

  62. 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.

    Article  CAS  Google Scholar 

  63. 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.

    Article  CAS  Google Scholar 

  64. 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.

    Article  CAS  PubMed  Google Scholar 

  65. 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.

    Article  CAS  PubMed  Google Scholar 

  66. 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.

    Article  CAS  Google Scholar 

  67. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. 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.

    Article  CAS  PubMed  Google Scholar 

  69. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. 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.

    Article  CAS  PubMed  Google Scholar 

  71. 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.

    Article  PubMed  Google Scholar 

  72. H. Jiang and B. Qiu, Photosynthetic adaptation of a bloom forming cyanobacterium Microcystis aeruginosa to prolonged UV-B exposure, J. Phycol., 2005, 41, 983.

    Article  Google Scholar 

Download references

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

  1. Dpto. Radiomicrobiología CAC, Comisión Nacional de Energía Atómica, Argentina

    Marcelo Hernando & Christian Houghton

  2. Área de Toxicología, Dpto. de Cs Biológicas, Facultad de Ciencias Exactas, UNLP, Argentina

    Melina Celeste Crettaz Minaglia, Darío Andrinolo, Daniela Sedan, Lorena Rosso & Leda Giannuzzi

  3. CONICET.Godoy Cruz, 2290, Buenos Aires, Argentina

    Melina Celeste Crettaz Minaglia, Darío Andrinolo, Daniela Sedan, Lorena Rosso & Leda Giannuzzi

  4. Fisico-Química - IBIMOL, UBA-CONICET, Argentina

    Gabriela Malanga

Authors
  1. Marcelo Hernando
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melina Celeste Crettaz Minaglia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriela Malanga
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christian Houghton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Darío Andrinolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Daniela Sedan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lorena Rosso
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Leda Giannuzzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcelo Hernando.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c7pp00265c

Search

Navigation