Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-13T01:49:58.050Z Has data issue: false hasContentIssue false
  • English
  • Français

Chemical compounds and antioxidant activity of Antarctic lichens

Published online by Cambridge University Press:  22 December 2021

Olga Kandelinskaya Open the ORCID record for Olga Kandelinskaya [Opens in a new window] ,
Helena Grischenko Open the ORCID record for Helena Grischenko [Opens in a new window] ,
Yury Hihinyak Open the ORCID record for Yury Hihinyak [Opens in a new window] ,
Mikhail Andreev Open the ORCID record for Mikhail Andreev [Opens in a new window] ,
Peter Convey Open the ORCID record for Peter Convey [Opens in a new window] ,
Dzmitry Lukashanets Open the ORCID record for Dzmitry Lukashanets [Opens in a new window] ,
Nikolai Kozel Open the ORCID record for Nikolai Kozel [Opens in a new window]  and
Ilya Prokopiev Open the ORCID record for Ilya Prokopiev [Opens in a new window]
Olga Kandelinskaya*
Affiliation:
V.F. KuprevichInstitute of Experimental Botany of National Academy of Sciences of Belarus, Akademicheskaya 27, 220072 Minsk, Belarus
Helena Grischenko
Affiliation:
V.F. KuprevichInstitute of Experimental Botany of National Academy of Sciences of Belarus, Akademicheskaya 27, 220072 Minsk, Belarus
Yury Hihinyak
Affiliation:
Scientific and Practical Center for Bioresources of National Academy of Sciences of Belarus, Akademicheskaya 27, 220072 Minsk, Belarus
Mikhail Andreev
Affiliation:
Komarov Botanical Institute of the Russian Academy of Sciences, Professor Popov St, 2, 197376, St Petersburg, Russia
Peter Convey
Affiliation:
British Antarctic Survey, NERC, High Cross, Madingley Road, Cambridge, CB3 0ET, UK Department of Zoology, University of Johannesburg, PO Box 524, Auckland Park 2006, South Africa
Dzmitry Lukashanets
Affiliation:
Scientific and Practical Center for Bioresources of National Academy of Sciences of Belarus, Akademicheskaya 27, 220072 Minsk, Belarus
Nikolai Kozel
Affiliation:
Institute of Biophysics and Cell Engineering of National Academy of Sciences of Belarus, Akademicheskaya 27, 220072 Minsk, Belarus
Ilya Prokopiev
Affiliation:
Institute of Biological Problems of Cryolithozone of the Siberian Branch of the Russian Academy of Sciences, Lenin Ave. 41, 677007, Yakutsk, Yakutia, Russia
*
okandy@yandex.ru
Get access Rights & Permissions [Opens in a new window]

Abstract

We assessed the content of some major and trace elements and lichen compounds as well as antioxidant activity in eight lichen species representing four families collected in areas > 1 km distant from Bellingshausen (King George Island) and > 1 km distant from Molodezhnaya (Thala Hills, Enderby Land) research stations. Content levels of Cu, Pb, Cd, Zn and As in Physcia caesia, Physconia muscigena, Umbilicaria aprina, Umbilicaria decussata and Usnea aurantiaco-atra thalli were similar to or lower than previously reported for these species in the Maritime and Continental Antarctic, as well as from reference sites. The first data on the contents of 15 elements in Ramalina terebrata and Thamnolecania brialmontii thalli from the Maritime Antarctic are reported. Our analyses confirmed the presence of the main photosynthetic pigments in the species examined (chlorophyll a and b, phaeophytin a and b, neoxanthin, violaxanthin, lutein and β-carotene). We identified protolichesterinic acid in T. brialmontii thalli for the first time. Antioxidant activity varied from 190 μg/g dry weight (U. decussata) to 14,740 μg/g dry weight (T. brialmontii). The data obtained complement previous research while also providing new baseline data that will have utility in monitoring and identifying future change.

Keywords

antioxidant capacitychemical elementsContinental Antarcticalichen substancesMaritime Antarcticphotosynthetic pigments
Type
Biological Sciences
Information
Antarctic Science , Volume 34 , Issue 1 , February 2022 , pp. 3 - 15
Check for updates
Copyright
Copyright © Antarctic Science Ltd 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Analytik Jena, AG. 2004. Determination of water- (ACW) and lipid- (ACL) soluble antioxidative capacity in plant extract. In Analytik Jena AG bioanalitical solutions. Jena, Analytik Jena, 1–8.Google Scholar
Andreev, M.P. 1988. The lichen flora of the King George Island. Novosti Sistematiki Nizshikh Rastenii, 25, 118–124. (in Russian).Google Scholar
Andreev, M.P. 2018. Lishajniki Antarktiki: vidovoj sostav, istoriya i perspektivy izucheniya i osobennosti formirovaniya sinuzij na ornitogennyh pochvah [Antarctic lichens: taxonomic composition, history and outlook of further study and the features of lichen synusia on ornithogenic soils]. In Budantsev, A.L. ed. Proceedings of the XIV Congress of the Russian Botanical Society and the conference ‘Botany in the Modern World’. Makhachkala: Alef, 3, 7–10. Retrieved from https://www.binran.ru/files/publications/Proceedings/Proceedings_RBO/XIV_RBO_Proceedings_T3.pdf (in Russian).Google Scholar
Armstrong, R.A. 2017. Adaptation of lichens to extreme conditions. In Shukla, V., Kumar, S. & Kumar, N., eds. Plant adaptation strategies in changing environment. Singapore, Springer, 1–27.Google Scholar
Bačkor, M. & Loppi, S. 2009. Interactions of lichens with heavy metals. Biologia Plantarum, 53, 10.1007/s10535-009-0042-y.CrossRefGoogle Scholar
Bajpai, R. & Upreti, D.K. 2012. Accumulation and toxic effect of arsenic and another heavy metals in a contaminated area of West Bengal, India, in the lichen Pyxine cocoes (Sw.) Nyl. Ecotoxicology and Environmental Safety, 83, 63–70.CrossRefGoogle Scholar
Balarinová, K., Barták, M., Hazdrová, J., Hájek, J. & Jílková, J. 2014. Changes in photosynthesis, pigment composition and glutathione contents in two Antarctic lichens during a light stress and recovery. Photosynthetica, 52, 10.1007/s11099-014-0060-7.CrossRefGoogle Scholar
Bargagli, R., Borghini, F. & Celesti, C. 2000. Elemental composition of the lichen Umbilicaria decussata. Italian Journal of Zoology, 67, 10.1080/11250000009356371.CrossRefGoogle Scholar
Bargagli, R., Iosco, F.P. & Barghigiani, C. 1987. Assessment of mercury dispersal in an abandoned mining area by soil and lichens analysis. Water, Air, and Soil Pollution, 36, 219–225.CrossRefGoogle Scholar
Bargagli, R., Battisti, E., Focardi, S. & Formichi, P. 1993. Preliminary data on environmental distribution of mercury in northern Victoria Land, Antarctic. Antarctic Science, 5, 3–8.CrossRefGoogle Scholar
Besco, E., Braccioli, E., Vertuani, S., Ziosi, P., Brazzo, F., Bruni, R. & Manfredini, S. 2007. The use of photochemiluminescence for the measurement of the integral antioxidant capacity of baobab products. Food Chemistry, 102, 10.1016/j.foodchem.2006.05.067.CrossRefGoogle Scholar
Boonpragob, K. 2002. Monitoring physiological change in lichens: total chlorophyll content and chlorophyll degradation. In Limis, P.L., Scheidegger, C. & Wolseley, P.A., eds. Monitoring with lichens - monitoring lichens. Berlin, Springer, 323–326.CrossRefGoogle Scholar
Boutron, C.F. & Wolff, E.W. 1989. Heavy metal and sulphur emissions to the atmosphere from human activities in Antarctica. 1967. Atmospheric Environment, 23, 10.1016/0004-6981(89)90051-6.Google Scholar
Braun, C., Mustafa, O., Nordt, A., Pfeiffer, S. & Peter, H.-U. 2012. Environmental monitoring and management proposals for the Fildes Region, King George Island, Antarctica. Polar Research, 31, 10.3402/polar.v31i0.18206.CrossRefGoogle Scholar
Bubach, D., Catán, S. P., Di Fonzo, C., Dopchiz, L., Arribére, M. & Ansaldo, M. 2016. Elemental composition of Usnea sp lichen from Potter Peninsula, 25 de Mayo (King George) Island, Antarctica. Environmental Pollution, 210, 10.1016/j.envpol.2015.11.045.CrossRefGoogle Scholar
Cazzonelli, C.I. 2011. Carotenoids in nature: insights from plants and beyond. Functional Plant Biology, 38, 10.1071/FP11192.CrossRefGoogle ScholarPubMed
Chettri, M.K., Sawidis, T. & Karataglis, S. 1997. Lichens as a tool for biogeochemical prospecting. Ecotoxicology and Environmental Safety, 38, 322–335.CrossRefGoogle ScholarPubMed
Convey, P. 2017. Antarctic ecosystems. Encyclopedia of Biodiversity, 10.1126/science.1104235.Google Scholar
Convey, P. & Peck, L.S. 2019. Antarctic environmental change and biological responses. Science Advances, 5, 10.1126/sciadv.aaz0888.CrossRefGoogle ScholarPubMed
Cornejo, A., Salgado, F., Caballero, J., Vargas, R., Simirgiotis, M. & Areche, C. 2016. Secondary metabolites in Ramalina terebrata detected by UHPLC/ESI/MS/MS and identification of parietin as tau protein inhibitor. International Journal of Molecular Sciences, 17, 10.3390/ijms17081303.CrossRefGoogle ScholarPubMed
Dolgikh, A.V., Mergelov, N.S., Abramov, A.A., Lupachev, A.V. & Goryachkin, S.V. 2015. Soils of Enderby Land. In Bockheim, J.G. ed. The soils of Antarctica. Berlin, Springer International Publishing, 45–53.CrossRefGoogle Scholar
Elix, J.A., Wirtz, N. & Lumbsch, H.T. 2007. Studies on the chemistry of some Usnea species of the Neuropogon group (Lecanorales, Ascomycota). Nova Hedwigia, 85, 10.1127/0029-5035/2007/0085-0491.CrossRefGoogle Scholar
Forni, E., Ghezzi, M. & Polesello, A. 1988. HPLC separation and fluorimetric estimation of chlorophylls and pheophytins in fresh and frozen peas. Chromatographia, 26, 10.1007/bf02268135.CrossRefGoogle Scholar
Fridel, T. & Büdel, B. 2008. Photobionts. In Nash, T.H. III, ed. Lichen biology. Cambridge, Cambridge University Press, 9–26.CrossRefGoogle Scholar
Garty, J. 2001. Biomonitoring atmospheric heavy metals with lichens: theory and application. Critical Reviews in Plant Sciences, 20, 10.1080/20013591099254.CrossRefGoogle Scholar
Garty, J., Ronen, R. & Galun, M. 1985. Correlation between chlorophyll degradation and the amount of some elements in the lichen Ramalina duriaei (de Not.) Jatta. Environmental and Experimental Botany, 25, 10.1016/0098-8472(85)90049-8.CrossRefGoogle Scholar
Golubkova, N.S., Savicz, V.P. & Simonov, I.M. 1968. Lichens of the western part of Enderby Land. Transactions of the Soviet Antarctic Expedition, 38, 247–253 (in Russian).Google Scholar
Huneck, S. & Yoshimura, I. 1996. Identification of lichen substances. In Huneck, S. & Yoshimura, I., eds. Identification of lichen substances. Berlin, Springer, 11–123.CrossRefGoogle Scholar
Kambar, Y., Vivek, M.N., Manasa, M., Prashith Kekuda, T.R. & Ramesh Kumar, K.A. 2014. Proximate and elemental analysis of Ramalina conduplicans Vain. (Ramalinaceae) and Parmotrema tinctorum (Nyl.) Hale (Parmeliacea). Journal of Chemical and Pharmaceutical Research, 6, 2668–2674.Google Scholar
Kandelinskaya, O.L., Gryshchenko, E.R., Ripinskaya, K.Y., Prokopiev, I.A., Filippova, G.V. & Bely, P.N. 2017. Biohimicheskie aspekty adaptivnoj strategii Cladonia stellaris [Biochemical aspects of the adaptive strategy of Cladonia stellaris]. Science and Innovations, 12, 65–69 (in Russian).Google Scholar
Kappen, L. 2000. Some aspects of the great success of lichens in Antarctica. Antarctic Science, 12, 10.1017/s0954102000000377.CrossRefGoogle Scholar
Kappen, L., Bölter, M. & Kühn, A. 1986. Field measurements of net photosynthesis of lichens in the Antarctic. Polar Biology, 5, 10.1007/bf00446094.CrossRefGoogle Scholar
Kurchenko, V.P., Bagmanyan, I.A., Myamin, V.E., Borodin, O.I. & Giginyak, Yu.G. 2016. The use of lichens for evaluation of heavy metal pollution of different regions of Antarctica. Proceedings of BSU, 11, 351–355.Google Scholar
Lagostina, E., Dal Grande, F., Andreev, M.P. & Printzen, C. 2018. The use of microsatellite markers for species delimitation in Antarctic Usnea subgenus Neuropogon. Mycologia, 110, 10.1080/00275514.2018.1512304.CrossRefGoogle ScholarPubMed
Lawrey, J.D. 1986. Biological role of lichen substances. The Bryologist, 89, 10.2307/3242751.CrossRefGoogle Scholar
Lee, J.S., Lee, H.K., Hur, J.-S., Andreev, M. & Hong, S.G. 2008. Diversity of the lichenized fungi in King George Island, Antarctica, revealed by phylogenetic analysis of partial large subunit rDNA sequences. Journal of Microbiology and Biotechnology, 18, 1016–1023.Google Scholar
Li, Y., Kromer, B., Schukraft, G., Bubenzer, O., Huang, M.-R., Wang, Z.-M., Bian, L.-G. & Li, C.-S. 2014. Growth rate of Usnea aurantiaco-atra (Jacq.) Bory on Fildes Peninsula, Antarctica and its climatic background. PLoS ONE, 9, 10.1371/journal.pone.0100735.Google Scholar
Lim, H.S. 2009. Heavy metal concentrations in the fruticose lichen Usnea aurantiacoatra from King George Island, South Shetland Islands, West Antarctica. Journal of the Korean Society for Applied Biological Chemistry, 52, 10.3839/jksabc.2009.086.CrossRefGoogle Scholar
Lohtander, K., Myllys, L., Källersjö, M., Moberg, R., Stenroos, S. & Tehler, A. 2009. New entities in Physcia aipolia-P. caesia group (Physciaceae, Ascomycetes): an analysis based on mtSSU, ITS, Group I Intron and betatubulin sequences. Annales Botanici Fennici, 46, 10.5735/085.046.0104.CrossRefGoogle Scholar
MacFarlane, J.D. & Kershaw, K.A. 1985. Some aspects of carbohydrate metabolism in lichens. In Brown, D.H., ed. Lichen physiology and cell biology. New York, Plenum Press, 1–8.Google Scholar
Maina, J.N. & Wang, Q. 2015. Seasonal response of chlorophyll a/b ratio to stress in a typical desert species: Haloxylon ammodendron. Arid Land Research and Management, 29, 10.1080/15324982.2014.980588.CrossRefGoogle Scholar
Manrique, E., Redondo, E.L., Seriña, E. & Izco, J. 1989. Estimation of chlorophyll degradation into phaeophytin in Anaptychia ciliaris as a method to detect air pollution. Lazaroa, 11, 141–148.Google Scholar
Markert, B. 1992. Establishing of reference plant for inorganic characterization of different plant species by chemical fingerprinting. Water, Air, and Soil Pollution, 64, 10.1007/bf00483363.CrossRefGoogle Scholar
Michel, R.F.M., Schaefer, C.E.G.R., Simas, F.N.B., Poelking, E.L. & Fernandes-Filho, E.I. 2010. Active layer thermal monitoring at two ice-free areas of King George Island, Maritime Antarctica. Symposium 1.1.1 Soil morphology and climate change. Proceedings of the 19th World Congress of Soil Science: Soil solutions for a changing world, Brisbane, Australia, 1–6 August 2010, 1–4. Retrieved from https://www.researchgate.net/publication/228534972.Google Scholar
Millbank, J.W. & Kershaw, K.A. 1973. Nitrogen metabolism. In Ahmadjian, V. & Hale, M., eds. The lichens. Cambridge, MA, Academic Press, 289–307.CrossRefGoogle Scholar
Moreira, A.S., Braz-Filho, R., Mussi-Dias, V. & Vieira, I.J. 2015. Chemistry and biological activity of Ramalina lichenized fungi. Molecules, 20, 10.3390/molecules20058952.CrossRefGoogle ScholarPubMed
Nash, T.H. III. 2008. Lichen biology. In Nash, T.H. III, ed. Lichen biology. Cambridge, Cambridge University Press, 299–314.CrossRefGoogle Scholar
Olech, M., Szymczyk, S. & Kajfosz, J. 1993. Local lead pollutions in the Antarctic region. Prace Minerologiczne, 83, 51–54 (in Polish with English summary).Google Scholar
Osyczka, P. & Olech, M. 2005. The lichen genus Cladonia of King George Island, South Shetland Islands, Antarctica. Polish Polar Research, 26, 107–123.Google Scholar
Osyczka, P., Dutkiewicz, E.M. & Olech, M. 2007. Trace elements concentrations in selected moss and lichen species collected within Antarctic research station. Polish Journal of Ecology, 55, 39–48.Google Scholar
Øvstedal, D.O. & Smith, R.I.L. 2001. Lichens of Antarctica and South Georgia: a guide to their identification and ecology. Cambridge, Cambridge University Press, 411 pp.Google Scholar
Pandey, V. & Upreti, D.K. 2000. Determination of heavy metals in lichens growing on different ecological habitats in Schirmacher Oasis, East Antarctica. Seventeenth Indian Expedition to Antarctica, Scientific Report Department of Ocean Development. Technical Publication, 15, 203–209.Google Scholar
Pawlik-Skowronska, B., di Toppi, L.S., Favali, M.A., Fossati, F., Pirszel, J. & Skowronski, T. 2002. Lichens respond to heavy metals by phytochelatin synthesis. New Phytologist, 156, 10.1046/j.1469-8137.2002.00498.x.CrossRefGoogle Scholar
Pegg, R.B., Amarowicz, R., Naczk, M. & Shahidi, F. 2007. PHOTOCHEM® for determination of antioxidant capacity of plant extracts. In Shahidi, F. & Ho, C.-T., eds. Antioxidant measurement and applications. Washington, DC, American Chemical Society, 140–158.CrossRefGoogle Scholar
Planchon, F.A.M., Boutron, C.F., Barbante, C., Cozzi, G., Gaspari, V., Wolff, E.W., et al. 2002. Changes in heavy metals in Antarctic snow from Coats Land since the mid-19th to the late-20th century. Earth and Planetary Science Letters, 200, 207–222.CrossRefGoogle Scholar
Poblet, A., Andradeb, S., Scagliola, M., Vodopivezd, C., Curtosid, A., Puccib, A. & Marcovecchioa, J. 1997. The use of epilithic Antarctic lichens (Usnea aurantiaco-atra and U. antartica) to determine deposition patterns of heavy metals in the Shetland Islands, Antarctica. Science of the Total Environment, 207, 187–194.CrossRefGoogle Scholar
Praveen Kumar, S.V., Prashith Kekuda, T.R., Vinayaka, K.S., Swathi, D., Mallikarjun, N. & Nishanth, B.C. 2010. Studies on proximate composition, antifungal and anthelmintic activity of a macrolichen Ramalina hossei H. Magn & G. Awasthi. International Journal of Biotechnology and Biochemistry, 6, 191–201.Google Scholar
Pregitzer, K.S. & King, J.S. 2005. Effects of soil temperature on nutrient uptake. In BassiriRad, H., ed. Nutrient acquisition by plants. Ecological studies (analysis and synthesis). Berlin, Springer, 277–310.CrossRefGoogle Scholar
Prokopiev, I.A., Poryadina, L.N., Filippova, G.V. & Shein, A.A. 2016. Soderzhanie vtorichnyh metabolitov v lishajnikah sosnovyh lesov Centralnoj Yakutii [Secondary metabolites content in pine forests lichens of central Yakutia]. Chemistry of Plant Raw Material, 3, 10.14258/jcprm.2016031174 (in Russian).Google Scholar
Rivera, M.S., Catan, S.P., Fonzo, C.D., Dopchiz, L., Arribere, M.A., Ansaldo, M., et al. 2018. Lichen as biomonitor of atmospheric elemental composition from Potter Peninsula, 25 de Mayo (King George) Island, Antarctica. Annals of Marine Science, 2, 10.17352/ams.000009.Google Scholar
Rola, K., Osyczka, P. & Kafel, A. 2016. Different heavy metal accumulation strategies of epilithic lichens colonising artificial post-smelting wastes. Archives of Environmental Contamination and Toxicology, 70, 10.1007/s00244-015-0180-5.CrossRefGoogle ScholarPubMed
RosStandart., 2011. Fodder, mixed fodder and animal feed raw stuff. Methods of nitrogen and crude protein determination. In GOST 13496.4-93. Moscow, StandartInform, 41–46 (in Russian).Google Scholar
Rudnic, R.L. & Gao, S. 2003. Composition of the continental crust. In Holland, H.D. & Turekian, K.K., eds. Treatise on geochemistry. London, Elsevier-Pergamon, 1–64.Google Scholar
Sadowsky, A. & Ott, S. 2016. Symbiosis as a successful strategy in continental Antarctica: performance and protection of Trebouxia photosystem II in relation to lichen pigmentation. Polar Biology, 39, 10.1007/s00300-015-1677-0.CrossRefGoogle Scholar
Sanchez-Hernandez, J.C. 2000. Trace element contamination in Antarctic ecosystems. Reviews of Environmental Contamination and Toxicology, 166, 83–127.Google ScholarPubMed
Sancho, L.G., Pintado, A. & Green, T.G.A. 2019. Antarctic studies show lichens to be excellent biomonitors of climate change. Diversity, 11, 10.3390/d11030042.CrossRefGoogle Scholar
Schroeter, B., Kappen, L., Green, T.G.A. & Seppelt, R.D. 1997. Lichens and the Antarctic environment; effects of temperature and water availability of photosynthesis. In Lyons, W.B., Howard-Williams, C. & Hawes, I., eds. Ecosystem processes in Antarctic ice-free landscapes. Rotterdam, A.A. Balkema, 103–117.Google Scholar
Smykla, J., Szarek-Gwiazda, E. & Krzewicka, B. 2005. Trace elements in the lichens Usnea aurantiaco-atra and Usnea antarctica from the vicinity of Uruguay's Artigas research station on King George Island, Maritime Antarctic. Polish Botanical Studies, 19, 49–57.Google Scholar
Taylor, S.R. 1964. Abundance of chemical elements in the continental crust: a new table. Geochimica et Cosmochimica Acta, 28, 10.1016/0016-7037(64)90129-2.CrossRefGoogle Scholar
Tyler, G. 1989. Uptake, retention and toxicity of heavy metals in lichens. Water, Air, and Soil Pollution, 47, 10.1007/bf00279330.CrossRefGoogle Scholar
Tyutereva, E.V., Ivanova, A.N. & Voitsekhovskaja, O.V. 2014. On the role of chlorophyll b in ontogenetic adaptations of plants. Biology Bulletin Reviews, 4, 10.1134/S2079086414060073.CrossRefGoogle Scholar
Upreti, D.K. & Pandev, V. 1994. Heavy metals of Antarctic lichens 1. Umbilicaria. Feddes Repertorium, 105, 10.1002/fedr.19941050312.CrossRefGoogle Scholar
Vlček, V., Pospíšilová, L. & Uhlík, P. 2017. Mineralogy and chemical composition of cryosols and andosols in Antarctica. Soil and Water Research, 13, 10.17221/231/2016-SWR.Google Scholar
Williams, L., Borchhardt, N., Colesie, C., Baum, C., Komsic-Buchmann, K., Rippin, M., et al. 2016. Biological soil crusts of Arctic Svalbard and of Livingston Island, Antarctica. Polar Biology, 40, 10.1007/s00300-016-1967-1.Google Scholar
Yamamoto, Y., Hara, K., Kawakami, H. & Komine, M. 2015. Lichen substances and their biological activities. Recent Advances in Lichenology, 2, 10.1007/978-81-322-2235-4_10.CrossRefGoogle Scholar
Supplementary material: File

Kandelinskaya et al. supplementary material

Kandelinskaya et al. supplementary material 1

Download Kandelinskaya et al. supplementary material(File)
File 20.3 KB
Supplementary material: File

Kandelinskaya et al. supplementary material

Kandelinskaya et al. supplementary material 2

Download Kandelinskaya et al. supplementary material(File)
File 14.7 KB
Supplementary material: File

Kandelinskaya et al. supplementary material

Kandelinskaya et al. supplementary material 3

Download Kandelinskaya et al. supplementary material(File)
File 19.7 KB
Supplementary material: PDF

Kandelinskaya et al. supplementary material

Kandelinskaya et al. supplementary material 4

Download Kandelinskaya et al. supplementary material(PDF)
PDF 321.9 KB