Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T13:12:03.830Z Has data issue: false hasContentIssue false

Low-temperature investigation of residual water bound in free-living Antarctic Prasiola crispa

Published online by Cambridge University Press:  01 November 2022

Magdalena Bacior*
Affiliation:
Department of Soil Science and Agrophysics, University of Agriculture in Kraków, Al. Mickiewicza 21, 31-120 Kraków, Poland
Hubert Harańczyk
Affiliation:
Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
Piotr Nowak
Affiliation:
Faculty of Computer Science, Electronics and Telecommunications, AGH University of Science and Technology, Al. Mickiewicza 30, 30-059 Kraków, Poland
Paulina Kijak
Affiliation:
Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
Monika Marzec
Affiliation:
Institute of Physics, Jagiellonian University, ul. Prof. Stanisława Łojasiewicza 11, 30-348 Kraków, Poland
Jakub Fitas
Affiliation:
Department of Mechanical Engineering and Agrophysics, University of Agriculture in Kraków, Al. Mickiewicza 21, 31-120 Kraków, Poland
Maria Olech
Affiliation:
Institute of Botany, Jagiellonian University, ul. Kopernika 27, 31-501 Kraków, Poland Institute of Biochemistry and Biophysics, Polish Academy of Sciences, ul. Pawińskiego 5a, 02-106 Warsaw, Poland

Abstract

Antarctic algae are extremophilic organisms capable of surviving harsh environmental conditions such as low temperatures and deep dehydration. Although these algae have various adaptations for life in extreme environments, the majority of the molecular mechanisms behind their resistance to dehydration and freezing are not yet fully understood. The aim of our research was to observe the behaviour of bound water freezing in the free-living Antarctic alga Prasiola crispa. One way to avoid frost damage involves deep dehydration of the algal thallus. For that reason, a detailed analysis of water freezing at different sample hydration levels was carried out. Nuclear magnetic resonance investigation revealed two types of water immobilization: cooperative bound water freezing for samples with sample hydration levels above Δm/m0 = 0.40 and non-cooperative bound water immobilization for lower thallus hydration levels. In the differential scanning calorimetry experiment, 2-h incubation at -20°C suggested the diffusion and final binding of supercooled water to the ice nuclei and a lower hydration level threshold, at which ice formation could be observed (Δm/m0 = 0.21). Our research provides a new perspective on water sorption and freezing in Antarctic algae, which may be important not only in biological systems, but also in such novel materials as metal-organic frameworks or covalent organic frameworks.

Type
Physical Sciences
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Antarctic Science Ltd

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

Angell, C.A. 1982. Supercooled water. In Franks, F., ed. Water and aqueous solutions at subzero temperatures. Water: a comprehensive treatise, vol. 7. New York: Plenum Press, 181.Google Scholar
Bacior, M., Nowak, P., Harańczyk, H., Patryas, S., Kijak, P. & Ligęzowaska, A. 2017. Extreme dehydration observed in Antarctic Turgidosculum complicatulum and in Prasiola crispa. Extremophiles, 21, 331343.CrossRefGoogle ScholarPubMed
Bacior, M., Harańczyk, H., Nowak, P., Kijak, P., Marzec, M., Fitas, J. & Olech, M.A. 2019. Low-temperature immobilization of water in Antarctic Turgidosculum complicatulum and in Prasiola crispa. Part I. Turgidosculum complicatulum. Colloid Surfaces B: Biointerfaces, 173, 869875.CrossRefGoogle ScholarPubMed
Becker, E.W. 1982. Physiological studies on Antarctic Prasiola crispa and Nostoc commune at low temperatures. Polar Biology, 1, 99104.Google Scholar
Benson, E., Harding, K. & Day, J.G. 2007. Algae at extremely low temperatures. In Seckbach, J., ed., Algae and cyanobacteria in extreme environments. Berlin: Springer, 365383.CrossRefGoogle Scholar
Bojic, S., Murray, A., Bentley, B.L., Spindler, R., Pawlik, P., Cordeiro, J.L., et al. 2021. Winter is coming: the future of cryopreservation. BMC Biology, 19, 56.CrossRefGoogle Scholar
Chang, T. & Zhao, G. 2021. Ice inhibition for cryopreservation: materials, strategies and challenges. Advanced Science, 8, 2002425.CrossRefGoogle ScholarPubMed
Chavhan, G.B., Babyn, P.S., Thomas, B., Shroff, M.M. & Haacke, E.M. 2009. Principles, techniques, and applications of T2*-based MR imaging and its special applications. Radiographics, 29, 14331449.CrossRefGoogle Scholar
Clarke, A., Morris, G.J., Fonesca, F., Murray, B.J. & Acton, E. 2013. A low temperature limit for life on Earth. PLoS One, 8, e66207.CrossRefGoogle ScholarPubMed
Determeyer-Wiedmann, N., Sadowsky, A., Convey, P. & Ott, S. 2019. Physiological life history strategies of photobionts of lichen species from Antarctic and moderate European habitats in response to stressful conditions. Polar Biology, 42, 395405.CrossRefGoogle Scholar
Duman, J.G. 2001. Antifreeze and ice nucleator proteins in terrestrial arthropods. Annual Review of Physiology, 63, 327357.CrossRefGoogle ScholarPubMed
Elster, J., Degma, P., Kováčik, L., Valentová, L., Šramowá, K. & Pereira, A.B. 2008. Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from the Antarctic, Arctic and Slovakia. Biologia, 63, 843851.CrossRefGoogle Scholar
Fernández-Marín, B., López-Pozo, M., Perera-Castro, A.V., Arzac, M.I., Saenz-Cenceros, A., Colesie, C., et al. 2019. Symbiosis at its limits: ecophysiological consequences of lichenization to the genus Prasiola in Antarctica. Annals of Botany, 20, 116.Google Scholar
Gao, Y., Zhang, Y., Yang, Y., Zang, J. & Gu, F. 2019. Molecular dynamics investigation of interfacial adhesion between oxidised bitumen and mineral surfaces, Applied Surface Science, 479, 449462.CrossRefGoogle Scholar
Graham, L.E., Graham, J.M. & Wilcox, L.W. 2009. Algae, 2nd edition. San Francisco, CA: Pearson Benjamin Cummings, 616 pp.Google Scholar
Gray, A., Krolikowski, M., Fretwell, P., Convey, P., Peck, L.S., Mendelowa, M., et al. 2021. Remote sensing phenology of Antarctic green and red snow algae using worldview satellites. Frontiers in Plant Science, 12, 671981.CrossRefGoogle ScholarPubMed
Hájek, J., Barták, M., Hadrová, J. & Forbelská, M. 2016. Sensitivity of photosynthetic processes to freezing temperature in extremophilic lichens evaluated by linear cooling and chlorophyll fluorescence. Cryobiology, 73, 329334.CrossRefGoogle ScholarPubMed
Hájek, J., Vaczi, P., Bartak, M. & Jahnova, L. 2012. Interspecific differences in cryoresistance of lichen symbiotic algae of genus Trebouxia assessed by cell viability and chlorophyll fluorescence. Cryobiology, 64, 215222.CrossRefGoogle ScholarPubMed
Harańczyk, H. 2003. On water in extremely dry biological systems. Post-doctoral dissertation, Jagiellonian University, 276 pp.Google Scholar
Harańczyk, H., Leja, A. & Strzałka, K. 2006. The effect of water accessible paramagnetic ions on subcellular structures formed in developing wheat photosynthetic membranes as observed by NMR and by sorption isotherm. Acta Physica Polonica A, 109, 389398.CrossRefGoogle Scholar
Harańczyk, H., Leja, A., Jemioła-Rzemińska, M. & Strzałka, K. 2009. Maturation processes of photosynthetic membranes observed by proton magnetic relaxation and sorption isotherm. Acta Physica Polonica A, 115, 526532.CrossRefGoogle Scholar
Harańczyk, H., Nowak, P., Lisowska, M., Florek-Wojciechowska, M., Lahuta, L.B. & Olech, M.A. 2016. A method of water-soluble solid fraction saturation concentration evaluation in dry thalli of Antarctic lichenized fungi, in vivo. Biochemistry and Biophysics Reports, 6, 226235.CrossRefGoogle Scholar
Harańczyk, H., Nowak, P., Bacior, M., Lisowska, M., Marzec, M., Florek, M. & Olech, M.A. 2012. Bound water freezing in Antarctic Umbilicaria aprina from Schirmacher Oasis. Antarctic Science, 24, 342352.CrossRefGoogle Scholar
Harańczyk, H., Strzałka, K., Kubat, K., Andrzejowska, A., Olech, M., Jakubiec, D., et al. 2021. A comparative analysis of gaseous phase hydration properties of two lichenized fungi: Niebla tigrina (Follman) Rundel & Bowler from Atacama Desert and Umbilicaria antarctica Frey & I. M. Lamb from Robert Island, Southern Shetlands Archipelago, Maritime Antarctica. Extremophiles, 25, 267283.Google Scholar
Heneghan, A.F. & Haymet, A.D.J. 2002. Liquid-to-crystal nucleation: improved lag-time apparatus to study supercooled liquids. Journal of Chemical Physics, 117, 53195327.CrossRefGoogle Scholar
Heneghan, A.F., Wilson, P.W. & Haymet, A.D. 2002. Statistics of heterogeneous nucleation of supercooled water, and the effect of an added catalyst. Proceedings of the National Academy of Sciences of the United States of America, 99, 96319634.CrossRefGoogle ScholarPubMed
Huiskes, A.H.L., Gremmen, N.J.M. & Francke, J.W. 1997. The delicate stability of lichen symbiosis: comparative studies on the photosynthesis of the lichen Mastodia tessellate and its free-living phycobiont, the alga Prasiola crispa. In Battaglia, B., Valencia, J. & Walton, D.W.H., eds., Antarctic communities: species, structure and survival. Cambridge: Cambridge University Press, 234240.Google Scholar
Inada, T., Zhang, X., Yabe, A. & Kozawa, Y. 2001. Active control of phase change from supercooled water to ice by ultrasonic vibration 1. Control of freezing temperature. International Journal of Heat and Mass Transfer, 44, 45234531.CrossRefGoogle Scholar
Jackson, A.E. & Seppelt, R.D. 1995. The accumulation of proline in Prasiola crispa during winter in Antarctica. Physiologia Plantarum, 94, 2530.CrossRefGoogle Scholar
Jackson, A.E. & Seppelt, R.D. 1997. Physiological adaptations to freezing and UV radiation exposure in Prasiola crispa, an Antarctic terrestrial alga. In Battaglia, B., Valencia, J. & Walton, D.W.H., eds., Antarctic communities: species, structure, and survival. Cambridge: Cambridge University Press, 226233.Google Scholar
Kawahara, H. 2013. Characterizations of functions of biological materials having controlling-ability against ice crystal growth. In Ferreira, S.O., ed., Advance topics on crystal growth. London: InTech, 119143.Google Scholar
Kosugi, M., Katashima, Y., Aikawa, S., Tanabe, Y., Kudoh, S., Kashino, Y., et al. 2010. Comparative study on the photosynthetic properties of Prasiola (Chlorophyceae) and Nostoc (Cyanophyceae) from Antarctic and non-Antarctic sites. Journal of Phycology, 46, 466746.CrossRefGoogle Scholar
Kovačik, L. & Pereira, A.B. 2001. Green alga Prasiola crispa and its lichenized form Mastodia tesselata in Antarctic environment: general aspects. Nova Hedwigia. Beiheft, 123, 465478.Google Scholar
Kovačik, L., Jancusova, M. & Pereira, A.B. 2003. Green alga Prasiola crispa (Lightf.) Menegh. and its lichenized form Turgidosculum complicatulum (Nyl.) J. Kohlm. & E. Kohlm. in Antarctic environment: variable of growth habit. In Olech, M.A., ed., The functioning of polar ecosystems as viewed against global environmental changes. Krakow: Institute of Botany, Jagiellonian University, 5156.Google Scholar
Lud, D., Huiskes, A.H.L. & Ott, S. 2001a. Morphological evidence for the symbiotic character of Turgidosculum complicatulum Kohlm. & Kohlm. (= Mastodia tesselata Hook.f, & Harvey). Symbiosis, 31, 141151.Google Scholar
Lud, D., Buma, A.G.J., Van de Poll, W., Moerdijk, T.C.W. & Huiskes, A.H.L. 2001b. DNA damage and photosynthetic performance in the Antarctic terrestrial alga Prasiola crispa ssp. antarctica (Chlorophyta) under manipulated UV-B radiation. Journal of Phycology, 37, 459467.Google Scholar
Nowak, P., Harańczyk, H., Kijak, P., Fitas, J., Lisowska, M., Baran, E. & Olech, M.A. 2018. Bound water behavior in Cetraria aculeata thalli during freezing. Polar Biology, 41, 865876.CrossRefGoogle Scholar
Pérez-Ortega, S., De Los Ríos, A., Crespo, A. & Sancho, L.G. 2010. Symbiotic lifestyle and phylogenetic relationships of the bionts of Mastodia tesselata (Ascomycota, incertae sedis). American Journal of Botany, 97, 738752.CrossRefGoogle Scholar
Richter, D., Matuła, J., Urbaniak, J., Waleron, M. & Czerwik-Marcinowska, J. 2017. Molecular, morphological and ultrastructural characteristics of Prasiola crispa (Lightfoot) Kützing (Chlorophyta) from Spitsbergen (Arctic). Polar Biology, 40, 379397.CrossRefGoogle Scholar
Santarius, K.A. 1992. Freezing of isolated thylakoid membranes in complex media. VIII. Differential cryoprotection by sucrose, proline and glycerol. Physiologia Plantarum, 84, 8793.Google Scholar
Storey, K.B. & Storey, J.M. 1996. Natural freezing survival in animals. Annual Review of Ecology, Evolution, and Systematics, 27, 365386.CrossRefGoogle Scholar
Tatur, A., Myrcha, A. & Niegodzisz, J. 1997. Formation of abandoned penguin rookery ecosystems in the maritime Antarctica. Polar Biology, 17, 405417.CrossRefGoogle Scholar
Valiullin, R. & Furo, I. 2002. The morphology of coexisting liquid and frozen phases in porous materials as revealed by exchange of nuclear spin magnetization followed by 1H nuclear magnetic resonance. Journal of Chemical Physics, 117, 23072316.Google Scholar
Wang, J., Xue, H., Zhou, B., Yao, Y.F. & Hansen, E.W. 2019. Interfacial water in mesopores and its implications to the surface features – a solid state NMR study. Applied Surface Science, 484, 11541160.CrossRefGoogle Scholar
Węglarz, W. & Harańczyk, H. 2000. Two-dimensional analysis of the nuclear relaxation function in the time domain: the program CracSpin. Journal of Physics D: Applied Physics, 33, 19091920.CrossRefGoogle Scholar
Wilson, P.W., Arthur, J.W. & Haymet, A.D.J. 1999. Ice premelting during differential scanning calorimetry. Biophysical Journal, 77, 28502855.CrossRefGoogle ScholarPubMed
Wilson, P.W., Heneghan, A.F. & Haymet, A.D.J. 2003. Ice nucleation in nature: supercooling point (SCP) measurements and the role of heterogeneous nucleation. Cryobiology, 46, 8898.CrossRefGoogle ScholarPubMed
Wolfe, J., Bryant, G. & Koster, K.L. 2002. What is ‘unfreezable water’, how unfreezable is it, and how much is there? CryoLetters, 23, 157166.Google Scholar
Zhang, Z.Q., Liu, H.L., Liu, Z., Zhang, Z., Cheng, G.G., Wang, X.D. & Ding, J.N. 2019. Anisotropic interfacial properties between monolayered black phosphorus and water. Applied Surface Science, 475, 857862.Google Scholar
Zhou, J., Liu, Y., Zhou, X., Ren, J. & Zhong, C. 2018. Magnetic multi-porous bio-adsorbent modified with amino siloxane for fast removal of Pb(II) from aqueous solution. Applied Surface Science, 427, 976985.CrossRefGoogle Scholar
Supplementary material: PDF

Bacior et al. supplementary material

Bacior et al. supplementary material

Download Bacior et al. supplementary material(PDF)
PDF 724.8 KB