SpringerLink
Log in

Morphological, Physiological, and Biochemical Traits of Melanized Thallus of the Cetraria islandica Lichen

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Lichens are extremophilic symbiotic associations possessing phenomenal resistance to abiotic stress-factors. In this regard, melanization of thalli in response to UV is one of the mechanisms protecting lichens from excessive insolation. However, microstructure and biochemical properties of the melanized thalli are still poorly investigated. In the present study, morphological, nanomechanical, and physiological, and biochemical traits of naturally melanized thalli of the Cetraria islandica (L.) Ach. lichen were examined. In the upper cortex of its thallus, the nature of the pigment layer was verified using typical qualitative reactions for melanins. It was found that melanization leads to changes in microstructure of the upper cortex of the mycobiont, in particular, thickening of the cell walls and extension of the interhyphal space. The melanized and pale (nonmelanized) thalli were found to differ from each other in their nanomechanical properties, including the parameters of adhesion and rigidity. This implies the possible formation of complex associates of melanin with cell wall components in the melanized mycobiont. In addition, higher antioxidant activity and lower respiratory activity were found in the melanized thalli of C. islandica in comparison with the pale thalli. Presumably, the found modifications in the microstructure and nanomechanical, physiological, and biochemical properties of thalli occurring in the course of melanization make lichens more resistant to intense insolation.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Brazil)

Instant access to the full article PDF.

Institutional subscriptions

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

REFERENCES

  1. Eisenreich, W., Knispel, N., and Beck, A., Advanced methods for the study of the chemistry and the metabolism of lichens, Phytochem. Rev., 2011, vol. 10, p. 445. https://doi.org/10.1007/s11101-011-9215-3

    Article  CAS  Google Scholar 

  2. Armstrong, R.A., Adaptation of lichens to extreme conditions, in Plant Adaptation Strategies in Changing Environment, Shukla, V., Kumar, S., and Kumar, N., Eds., Singapore: Springer, 2017, p. 27. https://doi.org/10.1007/978-981-10-6744-0_1

    Book  Google Scholar 

  3. Dadachova, E., Bryan, R.A., Howell, R.C., Schweitzer, A.D., Aisen, P., Nosanchuk, J.D., and Casadevall, A., The radioprotective properties of fungal melanin are a function of its chemical composition, stable radical presence and spatial arrangement, Pigm. Cell Melanoma Res., 2008, vol. 21, p. 192. https://doi.org/10.1111/j.1755-148X.2007.00430.x

    Article  CAS  Google Scholar 

  4. Huijser, A., Pezzella, A., and Sundström, V., Functionality of epidermal melanin pigments: Current knowledge on UV-dissipative mechanisms and research perspectives, Phys. Chem. Chem. Phys., 2011, vol. 13, p. 9119. https://doi.org/10.1039/C1CP20131J

    Article  PubMed  CAS  Google Scholar 

  5. Schweitzer, A.D., Revskaya, E., Chu, P., Pazo, V., Friedman, M., Nosanchuk, J.D., Cahill, S., Frases, S., Casadevall, A., and Dadachova, E., Melanin-covered nanoparticles for protection of bone marrow during radiation therapy of cancer, Int. J. Radiat. Oncol. Biol. Phys., 2010, vol. 78, p. 1494. https://doi.org/10.1016/j.ijrobp.2010.02.020

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Solhaug, K.A., Gauslaa, Y., Nybakken, L., and Bilger, W., UV-induction of sun-screening pigments in lichens, New Phytol., 2003, vol. 158, p. 91. https://doi.org/10.1046/j.1469-8137.2003.00708.x

    Article  CAS  Google Scholar 

  7. Daminova, A.G., Rogov, A.M., Rassabina, A.E., Beckett, R.P., and Minibayeva, F.V., Effect of melanization on thallus microstructure in the lichen Lobaria pulmonaria, J. Fungi, 2022, vol. 8, p. 791. https://doi.org/10.3390/jof8080791

    Article  CAS  Google Scholar 

  8. Daminova, A.G., Rassabina, A.E., Khabibrakhmanova, V.R., Beckett, R.P., and Minibayeva, F.V., Topography of UV-melanized thalli of Lobaria pulmonaria (L.) Hoffm., Plants, 2023, vol. 12, p. 2627. https://doi.org/10.3390/plants12142627

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Honegger, R. and Haisch, A., Immunocytochemical location of the (1→3) (1→4)-β-glucan lichenin in the lichen-forming ascomycete Cetraria islandica (Icelandic moss), New Phytol., 2001, vol. 150, p. 739. https://doi.org/10.1046/j.1469-8137.2001.00122.x

    Article  CAS  Google Scholar 

  10. Nybakken, L., Solhaug, K.A., Bilger, W., and Gauslaa, Y., The lichens Xanthoria elegans and Cetraria islandica maintain a high protection against UV-B radiation in Arctic habitats, Oecologia, 2004, vol. 140, p. 211. https://doi.org/10.1007/s00442-004-1583-6

    Article  PubMed  Google Scholar 

  11. Solhaug, K.A., Eiterjord, G., Løken, M.H., and Gauslaa, Y., Non-photochemical quenching may contribute to the dominance of the pale mat-forming lichen Cladonia stellaris over the sympatric melanic Cetraria islandica, Oecologia, 2024, vol. 204, p. 187.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Youngchim, S., Nosanchuk, J.D., Pornsuwan, S., Kajiwara, S., and Vanittanakom, N., The role of L-DOPA on melanization and mycelial production in Malassezia furfur, PLoS One, 2013, vol. 8, p. 1. https://doi.org/10.1371/journal.pone.0063764

    Article  CAS  Google Scholar 

  13. Rejniak, J., New method of melanin staining in histological preparations, Pathol. Pol., 1956, vol. 7, p. 101.

    CAS  Google Scholar 

  14. Lillie, R.D., A Nile blue staining technic for the differentiation of melanin and lipofuscins, Stain Technol., 1956, vol. 31, p. 151.

    Article  PubMed  CAS  Google Scholar 

  15. Viktorova, L.V., Galeeva, E.I., and Minibayeva, F.V., Laccases and tyrosinases in lichen thalli Lobaria pulmonaria (L.) Hoffm., Ekobiotekh., 2020, vol. 3, p. 220. https://doi.org/10.31163/2618-964X-2020-3-2-220-228

  16. Bellincampi, D., Dipperro, N., Salvi, G., Gervcone, F., and De Lorenzo, G., Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants, Plant Physiol., 2000, vol. 122, p. 1379. https://doi.org/10.1104/pp.122.4.1379

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Valitova, Y.N., Khabibrahmanova, V.R., Guryanov, O.P., Uvaeva, V.L., Khairullina, A.F., Rakhmatullina, D.F., Galeeva, E.I., Trifonova, T.V., Viktorova, L.V., and Minibaeva, F.V., Changes in the lipid composition of the lichen Peltigera canina under the influence of elevated temperature, Izv. Vuzov. Prikl. Khim. Biotekhnol., 2023, vol. 3, p. 532. https://doi.org/10.21285/2227-2925-2023-13-4-532-544

    Article  Google Scholar 

  18. Słominski, A., Moellmann, G., Kuklinska, E., Bomirski, A., and Pawelek, J., Positive regulation of melanin pigmentation by two key substrates of the melanogenic pathway, L-tyrosine and L-dopa, J. Cell Sci., 1988, vol. 89, p. 287. https://doi.org/10.1242/jcs.89.3.287

    Article  PubMed  Google Scholar 

  19. Nash, T.H., Lichen Biology, Cambridge: Cambridge University Press, 2008, 2nd Ed. https://doi.org/10.1017/CBO9780511790478

    Book  Google Scholar 

  20. Butler, M.J. and Day, A.W., Fungal melanins: A review, Can. J. Microbiol., 1998, vol. 44, p. 1115. https://doi.org/10.1139/w98-119

    Article  CAS  Google Scholar 

  21. Jacobson, E.S., Pathogenic roles for fungal melanins, Clin. Microbiol. Rev., 2000, vol. 13, p. 708. https://doi.org/10.1128/cmr.13.4.708

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Pacelli, C., Bryan, R.A., Onofri, S., Selbmann, L., Zucconi, L., Shuryak, I., and Dadachova, E., The effect of protracted X-ray exposure on cell survival and metabolic activity of fast and slow growing fungi capable of melanogenesis, Environ. Microbiol. Rep., 2018, vol. 10, p. 255. https://doi.org/10.1111/1758-2229.12632

    Article  PubMed  CAS  Google Scholar 

  23. Pavan, M.E., López, N.I., and Pettinari, M.J., Melanin biosynthesis in bacteria, regulation and production perspectives, Appl. Microbiol. Biotechnol., 2020, vol. 104, p. 1357. https://doi.org/10.1007/s00253-019-10245-y

    Article  PubMed  CAS  Google Scholar 

  24. Choi, K.-Y., Bioprocess of microbial melanin production and isolation, Front. Bioeng. Biotechnol., 2021, vol. 9, p. 1. https://doi.org/10.3389/fbioe.2021.765110

    Article  Google Scholar 

  25. Raposo, G. and Marks, M.S., Melanosomes—dark organelles enlighten endosomal membrane transport, Nat. Rev. Mol. Cell Biol., 2007, vol. 8, p. 786. https://doi.org/10.1038/nrm2258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Yoshikawa-Murakami, C., Mizutani, Y., Ryu, A., Naru, E., Teramura, T., Homma, Y., and Fukuda, M., A novel method for visualizing melanosome and melanin distribution in human skin tissues, Int. J. Mol. Sci., 2020, vol. 21, p. 8514. https://doi.org/10.3390/ijms21228514

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Rassabina, A.E., Guryanov, O.P., Beckett, R.P., and Minibayeva, F.V., Melanin of lichens Cetraria islandica and Pseudevernia furfuracea: structural features and physical and chemical properties, Biochem. (Moscow), 2020, vol. 85, p. 729.

    Article  Google Scholar 

  28. Rassabina, A.E., Khabibrakhmanova, V.R., Babaev, V.M., Daminova, A.G., and Minibayeva, F.V., Melanins from the lichens Lobaria pulmonaria and Lobaria retigera as ecofriendly adsorbents of synthetic dyes, Int. J. Mol. Sci., 2022, vol. 23, p. 15605. https://doi.org/10.3390/ijms232415605

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Khabibrahmanova, V.R., Rassabina, A.E., Khairullina, A.F., and Minibayeva, F.V., Physico-chemical characteristics and antioxidant properties of melanins isolated from lichen Leptogium furfuraceum (Harm.), Khim. Rast. Syrya, 2022, vol. 4, p. 115.

    Google Scholar 

  30. Gauslaa, Y., Alam, M.A., Lucas, P.L., Chowdhury, D.P., and Solhaug, K.A., Fungal tissue per se is stronger as a UV-B screen than secondary fungal extrolites in Lobaria pulmonaria, Fungal Ecol., 2017, vol. 26, p. 109. https://doi.org/10.1016/j.funeco.2017.01.005

    Article  Google Scholar 

  31. Mafole, T.C., Solhaug, K.A., Minibayeva, F.V., and Beckett, R.P., Occurrence and possible roles of melanic pigments in lichenized ascomycetes, Fungal Biol. Rev., 2019, vol. 33, p. 159. https://doi.org/10.1016/j.fbr.2018.10.002

    Article  Google Scholar 

  32. Mostert, A.B., Powell, B.J., Pratt, F.L., Hanson, G.R., Sarna, T., Gentle, I.R., and Meredith, P., Role of semiconductivity and ion transport in the electrical conduction of melanin, PNAS, 2012, vol. 109, p. 8943. https://doi.org/10.1073/pnas.1119948109

    Article  PubMed  PubMed Central  Google Scholar 

  33. Siletti, C.E., Zeiner, C.A., Bhatnagar, J.M., Distributions of fungal melanin across species and soils, Soil Biol. Biochem., 2017, vol. 113, p. 285. https://doi.org/10.1016/j.soilbio.2017.05.030

    Article  CAS  Google Scholar 

Download references

Funding

The work was supported by the Russian Science Foundation, project no. 23-14-00327, Analysis of Morphology and Topography of Melanized Thalli (for A. Daminova and F. Minibayeva). This work was partially performed within the framework of the government assignment of the FRC Kazan Scientific Center of RAS and supported by the Kazan Federal University Strategic Academic Leadership Program (PRIORITY-2030 for F. Minibayeva).

Author information

Authors and Affiliations

  1. Kazan Institute of Biochemistry and Biophysics, Kazan Scientific Center, Academy of Sciences, 420111, Kazan, Russia

    A. G. Daminova, E. I. Galeeva, D. F. Rakhmatullina, L. V. Viktorova & F. V. Minibayeva

  2. “Biomarker” Research Laboratory, Institute of Fundamental Medicine and Biology, Kazan Federal University, 420008, Kazan, Russia

    F. V. Minibayeva

Authors
  1. A. G. Daminova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. I. Galeeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. F. Rakhmatullina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. V. Viktorova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. V. Minibayeva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. G. Daminova.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

Additional information

Translated by A. Aver’yanov

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Daminova, A.G., Galeeva, E.I., Rakhmatullina, D.F. et al. Morphological, Physiological, and Biochemical Traits of Melanized Thallus of the Cetraria islandica Lichen. Russ J Plant Physiol 71, 92 (2024). https://doi.org/10.1134/S1021443724606104

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1134/S1021443724606104

Keywords:

Search

Navigation