The first phylogenetic and ecophysiological characterisation of Ankistrodesmus antarcticus CCAP 202/25, an Antarctic green alga isolated from freshwater ice

Vol.14,No.2(2024)

Abstract

Glacier ice algae and snow algae are important primary producers in extreme cold environments and significantly impact global processes through their role in carbon cycling and glacier melting by reducing surface albedo. These organisms have evolved unique cold-adaptation mechanisms, making them promising candidates for biotechnological applications, yet few species are characterised in detail. Such studies are also becoming particularly urgent, as polar cryospheric habitats are rapidly changing because of the ongoing climate change. Here we describe the phylogenetic placement and ecophysiological characterisation of the strain Ankistrodesmus antarcticus CCAP 202/25 that was isolated from a sample of green-coloured icicle collected on Sabrina Island (Balleny Islands, Antarctica). Cells maintained the size and shape that were reported in the original description of the strain in 1968. Analysis of the 18S rDNA confirmed its placement in the Selenastraceae family and, more specifically, in the highly supported and ecologically diversified Monoraphidium V clade, suggesting that a revision of its taxonomic assignment to the genus Ankistrodesmus will be necessary. Comparison of secondary structures of ITS2 rDNA uncovered several closely related strains with diverse or unknown origin that should be regarded as conspecific with Ankistrodesmus antarcticus CCAP 202/25. Therefore, more data are necessary to get a detailed insight into the phylogenetic and ecological diversification within this group. The cultivation of the strain in crossed gradients of temperature and light reflected adaptation of the species to cold Antarctic habitats. Similarly to psychrophilic species, Ankistrodesmus antarcticus was able to grow at 1°C, but the highest growth rates were recorded in a wide range of temperature (6–25°C) making its ecophysiological classification difficult. The ability of the species to utilise very low intensity (and simultaneously wide range) of photosynthetically active radiation also indicates its adaptation to a polar cryospheric habitat, where light availability can often represent the limiting factor, but significant fluctuations of irradiance can be common, both short-term and long-term.


Keywords:
Ankistrodesmus; Antarctica; Chlorophyta; freshwater ice; irradiance; Selenastraceae; temperature
References

Bischoff, H. W., Bold, H. C. (1963): Some soil algae from Enchanted Rock and related algal species. Phycological Studies IV. – University of Texas Publications: 6318, pp. 1–95.

Butler, H. G., Edworthy, M. G. and EllisEvans, J. C. (2000): Temporal plankton dynamics in an oligotrophic maritime Antarctic lake. Freshwater Biology, 43: 215-230.

Cao, K., He, M., Yang, W., Chen, B., Luo, W., Zou, S. and Wang, C. (2016): The eurythermal adaptivity and temperature tolerance of a newly isolated psychrotolerant Arctic Chlorella sp. Journal of Applied Phycology, 28: 877-888.

Coleman, A.W. (2007): Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Research, 35: 3322-3329.

Cota, G. F. (1985): Photoadaptation of high Arctic ice algae. Nature, 315: 219-222.

Da Silva, T. G., Bock, C., Sant’Anna, C. L., Bagatini, I. L., Wodniok, S. and Vieira, A. A. H. (2017): Selenastraceae (Sphaeropleales, Chlorophyceae): rbcL, 18S rDNA and ITS-2 secondary structure enlightens traditional taxonomy, with description of two new genera, Messastrum gen. nov. and Curvastrum gen. nov. Fottea, 17: 1-19.

Darty, K., Denise, A. and Ponty, Y. (2009): VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics, 25: 1974-1975.

Davey, M. P., Norman, L., Sterk, P., Huete-Ortega, M., Bunbury, F., Loh, B. K. W., Stockton, S., Peck, L. S., Convey, P., Newsham, K. K. and Smith, A. G. (2019): Snow algae communities in Antarctica: Metabolic and taxonomic composition. New Phytologist, 222: 1242-1255.

Fawley, M. W., Dean, M. L., Dimmer, S. K. and Fawley, K. P. (2005): Evaluating the morphospecies concept in the Selenastraceae (Chlorophyceae, Chlorophyta). Journal of Phycology, 42: 142-154.

Giudice, A. L., Rizzo, C. (2020). Culture collections as hidden sources of microbial biomolecules and biodiversity. Diversity, 12(7): 264.

Halldal, P., French, C. S. (1958): Algal growth in the crossed gradients of light and temperature. Physiologia Plantarum, 11: 401-420.

Hamby, R. K., Sims, L., Issel, L. and Zimmer, E. (1988): Direct ribosomal RNA sequencing: Optimization of extraction and sequencing methods for work with higher plants. Plant Molecular Biology Reporter, 6: 175-192.

Hindák, F. (1963): Systematik der Gattungen Koliella gen. nov. und Raphidonema Lagerh. Nova Hedwigia, 6: 95-125.

Hoham, R. W., Remias, D. (2020): Snow and glacial algae. Journal of Phycology, 56: 264-282.

Izaguirre, I., Mataloni, G., Allende, L. and Vinocur, A. (2001): Summer fluctuations of microbial planktonic communities in a eutrophic lake – Cierva Point, Antarctica. Journal of Plankton Research, 23: 1095-1109.

Izaguirre, I., Allende, L. and Marinone, M. C. (2003): Comparative study of the planktonic communities of three lakes of contrasting trophic status at Hope Bay (Antarctic Peninsula). Journal of Plankton Research, 25: 1079-1097.

Katana, A., Kwiatowski, J., Spalik, K., Zakryś, B., Szalacha, E. and Szymańska, H. (2001): Phylogenetic position of Koliella (Chlorophyta) as inferred from nuclear and chloroplast small subunit rDNA. Journal of Phycology, 37: 443-451.

Kol, E. (1926): Über ein neues Mitglied des Kryoplanktons der Hohen Tatra Ankistrodesmus tatrae Kol nova species. Acta Societatis Botanicorum Poloniae, 4: 166-168.

Kol, E. (1971): Green snow and ice from the Antarctica. Annales Historico-Naturales Musei Nationalis Hungarici, 63: 51-56.

Kol, E., Flint, E. A. (1968): Algae in green ice from the Balleny Islands, Antarctica. New Zealand Journal of Botany, 6: 249-261.

Komárková-Legnerová, J. (1969): The systematics and ontogenesis of the genera Ankistrodesmus Corda and Monoraphidium gen. nov. In: Fott, B. (Ed.): Studies in Phycology. Academia, Prague, pp. 75–144.

Krienitz, L., Bock, C. (2012): Present state of the systematics of planktonic coccoid green algae of inland waters. Hydrobiologia, 698: 295-326.

Krienitz, L., Ustinova, I., Friedl, T. and Huss, V. A. (2001): Traditional generic concepts versus 18S rRNA gene phylogeny in the green algal family Selenastraceae (Chlorophyceae, Chlorophyta). Journal of Phycology, 37: 852-865.

Krienitz, L., Bock, C., Nozaki, H. and Wolf, M. (2011): SSU rRNA gene phylogeny of morphospecies affiliated to the bioassay alga “Selenastrum capricornutum” recovered the polyphyletic origin of crescent-shaped Chlorophyta. Journal of Phycology, 47: 880-893.

Kvíderová, J. (2010): Rapid algal toxicity assay using variable chlorophyll fluorescence for Chlorella kessleri (Chlorophyta). Environmental Toxicology, 25: 554-563.

Kvíderová, J., Henley, W. J. (2005): The effect of ampicillin plus streptomycin on growth and photosynthesis of two halotolerant chlorophyte algae. Journal of Applied Phycology, 17: 301-307

Kvíderová, J., Lukavský, J. (2001): Gradients – basic character of the environment and possibilities of their modeling in the laboratory. Czech Phycology, 1: 77-85.

Laybourn-Parry, J., Tranter, M. and Hodson, A. J. (2012): The ecology of snow and ice environments. Oxford University Press, 179 p.

McKnight, D. M., Howes, B. L., Taylor, C. D. and Goehringer, D. D. (2000): Phytoplankton dynamics in a stably stratified Antarctic lake during winter darkness. Journal of Phycology, 36: 852-861.

Morgan-Kiss, R. M., Priscu, J. C., Pocock, T., Gudynaite-Savitch, L. and Huner, N. P. (2006): Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiology and Molecular Biology Reviews, 70: 222-252.

Morita, R. Y. (1975): Psychrophilic bacteria. Bacteriological Reviews, 39: 144-167.

Nedbalová, L., Mihál, M., Kvíderová, J., Procházková, L., Řezanka, T. and Elster, J. (2017): Identity, ecology and ecophysiology of planktic green algae dominating in ice-covered lakes on James Ross Island (northeastern Antarctic Peninsula). Extremophiles, 21: 187-200.

Posada, D. (2008): jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25: 1253-1256.

Procházková, L., Leya, T., Křížková, H. and Nedbalová, L. (2019): Sanguina nivaloides and Sanguina aurantia gen. et spp. nov. (Chlorophyta): The taxonomy, phylogeny, biogeography and ecology of two newly recognised algae causing red and orange snow. FEMS Microbiology Ecology, 95: fiz064.

Remias, D., Procházková, L., Nedbalová, L., Benning, L. G. and Lutz, S. (2023): Novel insights in cryptic diversity of snow and glacier ice algae communities combining 18S rRNA gene and ITS2 amplicon sequencing. FEMS Microbiology Ecology, 99: fiad134.

Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. and Huelsenbeck, J. P. (2012): Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61: 539-542.

Řezanka, T., Nedbalová, L., Lukavský, J., Střížek and Sigler, K. (2017): Pilot cultivation of the green alga Monoraphidium sp. producing a high content of polyunsaturated fatty acids in a low-temperature environment. Algal Research, 22: 160-165.

Reynolds C. S. (2006): Growth and replication of phytoplankton. In: Reynolds C. S.: The Ecology of Phytoplankton. Ecology, Biodiversity and Conservation. Cambridge University Press, pp. 178–238.

Seaburg, K. G., Parked, B. C., Wharton, R. A. and Simmons, G. M. (1981): Temperature-growth responses of algal isolates from antarctic oases. Journal of Phycology, 17: 353-360.

Seibel, P. N., Müller, T., Dandekar, T., Schultz, J. and Wolf, M. (2006): 4SALE – a tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinformatics, 7: 498.

Seibel, P. N., Müller, T., Dandekar, T. and Wolf, M. (2008) Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE. BMC Research Notes, 1: 91.

Solovchenko, A., Selyakh, I., Semenova, L.Scherbakov, P., Zaytseva, A., Zaytsev, P., Fedorenko, T., Alam, M. A., Jingliang, X., Lukyanov, A., Mikhaуlova, E. and Lobakova E. (2024): A local or a stranger? Comparison of autochthonous vs. allochthonous microalgae potential for bioremediation of coal mine drainage water. Chemosphere, 365: 143359.

Soto, D. F., Fuentes, R., Huovinen, P. and Gómez, I., (2020): Microbial composition and photosynthesis in Antarctic snow algae communities: Integrating metabarcoding and pulse amplitude modulation fluorometry. Algal Research, 45: 101738.

Teoh, M. L., Chu, W. L., Marchant, H. and Phang, S. M. (2004): Influence of culture temperature on the growth, biochemical composition and fatty acid profiles of six Antarctic microalgae. Journal of Applied Phycology, 16: 421-430.

White, T. J., Bruns, T., Lee, S. and Taylor, J. (1990): Amplification and direct sequencing of fungal ribosomal RNA Genes for phylogenetics. In: M. A. Innis, D. H. Gelfand, J. J. Sninsky and T. J. White (Eds.): PCR protocols: A guide to methods and applications (Vol. 18, pp. 315–322) London: Academic Press.

Wolf, M., Chen, S., Song, J., Ankenbrand, M. and Müller, T. (2013): Compensatory base changes in ITS2 secondary structures correlate with the biological species concept despite intragenomic variability in ITS2 sequences – a proof of concept. PloS One, 8: e66726.

Yee, W. (2016): Microalgae from the Selenastraceae as emerging candidates for biodiesel production: A mini review. World Journal of Microbiology and Biotechnology, 32(4): 64.

Zuker, M. (2003): Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31: 3406-3415.

Zwickl, D. J. (2006): Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas at Austin. Retrieved from www.bio.utexas.edu/faculty/antisense/garli/Garli.html

Web sources / Other sources

[1] http://mfold.rna.albany.edu/?q5mfold

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