Unveiling the molecular mechanisms of the stress resilience of High Arctic Klebsormidium flaccidum: a multifaceted study

. 2025 Oct 22 ; 66 (10) : 1397-1411.

Jazyk angličtina Země Japonsko Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40794876

Grantová podpora
BE1779/25-1 Deutsche Forschungsgemeinschaft
22-08680L Czech Science Foundation
67985939 Czech Academy of Sciences
University Research Centers
UNCE/24/SCI/006 Charles University
Czech Academy of Sciences

The green alga Klebsormidium is found worldwide in terrestrial and freshwater habitats. A novel strain was isolated from biological soil crusts on Breinosa Mountain in Svalbard (High Arctic, 78°N) to investigate its adaptation to extreme Arctic conditions, characterized by low temperatures and short periods of snow-free ground. Genetic analyses confirmed the strain's identity as Klebsormidium flaccidum, showing high genetic similarity to strains from polar and temperate habitats. This study explored the effects of nitrogen starvation, cold stress, desiccation, and freezing, focusing on molecular responses and stress resilience. Nitrogen starvation strongly impacted metabolic activity, while cold and desiccation stress had more subtle effects, with K. flaccidum showing permanent stress-related gene expression instead of acute responses. Cold acclimation was found to enhance desiccation and freezing tolerance, while nitrogen starvation worsened the effects of these stresses. These results suggest that K. flaccidum CCALA 1182 is inherently capable of withstanding fluctuating environmental stresses, highlighting its potential for survival in diverse and harsh ecosystems.

Zobrazit více v PubMed

Aigner, S., Arc, E., Schletter, M., Karsten, U., Holzinger, A. and Kranner, I. (2022) Metabolite profiling in green microalgae with varying degrees of desiccation tolerance. Microorganisms  10:1–18. PubMed PMC

Arzac, M.I., Miranda-Apodaca, J., Gasulla, F., Arce-Guerrero, M., Fernández-Marín, B. and García-Plazaola, J.I. (2023) Acquisition of desiccation tolerance unveiled: polar lipid profiles of streptophyte algae offer insights. Physiol. Plant.  175:e14073. PubMed

Becker, B. and Marin, B. (2009) Streptophyte algae and the origin of embryophytes. PubMed PMC

Becker, B., Feng, X., Yin, Y. and Holzinger, A. (2020) Desiccation tolerance in streptophyte algae and the algae to land plant transition: evolution of LEA and MIP protein families within the Viridiplantae. J. Exp. Bot.  71:3270–3278. PubMed PMC

Bolger, A.M., Lohse, M. and Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics  30:2114–2120. PubMed PMC

Buchfink, B., Reuter, K. and Drost, H.G. (2021) Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. Methods  18:366–368. PubMed PMC

Curran, J., Driver, F., Ballard, J.W.O. and Milner, R.J. (1994) Phylogeny of

Day, J.G., Iorenz, M., Wilding, T.A., Friedl, T., Harding, K., Pröschold, T., et al. (2007) The use of physical and virtual infrastructures for the validation of algal cryopreservation methods in international culture collections. CryoLetters  28:359–376. PubMed

Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., et al. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics  29:15–21. PubMed PMC

Dreyling, L., Schmitt, I. and Dal Grande, F. (2022) Tree size drives diversity and community structure of microbial communities on the bark of beech (

Elster, J. and Benson, E.E. (2004) Life in the polar terrestrial environment with a focus on algae and cyanobacteria. In: Fuller, B, Lane, N and Benson, EE (eds) Life in the Frozen State. Taylor and Francis, London, UK, pp 111–149.

Elster, J., Degma, P., Kováčik, Ľ., Valentová, L., Šrámková, K. and Pereira, A.B. (2008a) Freezing and desiccation injury resistance in the filamentous green alga

Elster, J., Lukavsky, J., Harding, K., Benson, E.E. and Day, J.G. (2008b) Deployment of the encapsulation-dehydration protocol to cryopreserve polar microalgae held at the Czech Republic Academy of Sciences Institute of Botany. CryoLetters  29:27–28. PubMed

Ettl, H. and Gärtner, G. (1988) Süßwasserflora von Mitteleuropa, Vol. 10. G. Fischer Verlag, Jena, Germany, p 437.

Fu, L., Niu, B., Zhu, Z., Wu, S. and Li, W. (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics  28:3150–3152. PubMed PMC

Glaser, K., Van, A.T., Pushkareva, E., Barrantes, I. and Karsten, U. (2022) Microbial communities in biocrusts are recruited from the neighboring sand at coastal dunes along the Baltic Sea. PubMed PMC

Götz, S., Garcia-Gomez, J.M., Terol, J., Williams, T.D., Nagaraj, S.H., Nueda, M.J., et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. PubMed PMC

Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. PubMed PMC

Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., et al. (2013) A. De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. PubMed PMC

Hammer, Ø., Harper, D. and Ryan, P. (2001) PAST: paleontological statistics software package for education and data analysis.

Holzinger, A., Lütz, C. and Karsten, U. (2011) Desiccation stress causes structural and ultrastructural alterations in the aeroterrestrial green alga PubMed

Holzinger, A., Kaplan, F., Blaas, K., Zechmann, B., Komsic-Buchmann, K. and Becker, B. (2014) Transcriptomics of desiccation tolerance in the streptophyte green alga PubMed PMC

Holzinger, A., Plag, N., Karsten, U. and Glaser, K. (2023) Terrestrial PubMed PMC

Hori, K., Maruyama, F., Fujisawa, T., Togashi, T., Yamamoto, N., Seo, M., et al. (2014) PubMed PMC

Huerta-Cepas, J., Szklarczyk, D., Heller, D., Hernández-Plaza, A., Forslund, S.K., Cook, H., et al. (2019) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. PubMed PMC

Jones, P., Binns, D., Chang, H.-Y., Fraser, M., Li, W., McAnulla, C., et al. (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics  30:1236–1240. PubMed PMC

Kanehisa, M. and Goto, S. (2000) KEGG: Kyoto encyclopedia of genes and genomes. PubMed PMC

Karsten, U., Herburger, K. and Holzinger, A. (2016) Photosynthetic plasticity in the green algal species PubMed PMC

Kiss, É., Talbot, J., Adams, N.B.P., Opekar, S., Moos, M., Pilný, J., et al. (2023) Chlorophyll biosynthesis under the control of arginine metabolism. PubMed PMC

Kopylova, E., Noé, L. and Touzet, H. (2012) SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics  28:3211–3217. PubMed

Kriventseva, E.V., Kuznetsov, D., Tegenfeldt, F., Manni, M., Dias, R., Simao, F.A., et al. (2019) OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial, and viral genomes for evolutionary and functional annotations of orthologs. PubMed PMC

Li, W. and Godzik, A. (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics  22:1658–1659. PubMed

Lokhorst, G.M. (1996) Comparative taxonomic studies on the genus

Manasa, S.L., Panigrahy, M., Panigrahi, K.C.S. and Rout, G.R. (2022) Overview of cold stress regulation in plants.

Marin, B., Klingberg, M. and Melkonian, M. (1998) Phylogenetic relationships among the cryptophyta: analyses of nuclear-encoded SSU rRNA sequences support the monophyly of extant plastid-containing lineages. Protist  149:265–276. PubMed

Mikhailyuk, T.I., Sluiman, H.J., Massalski, A., Mudimu, O., Demchenko, E.M., Kondratyuk, S.Y., et al. (2008) New streptophyte green algae from terrestrial habitats and an assessment of the genus PubMed

Mikhailyuk, T., Glaser, K., Holzinger, A. and Karsten, U. (2015) Biodiversity of PubMed PMC

Mugnai, G., Pinchuk, I., Borruso, L., Tiziani, R., Sannino, C., Canini, F., et al. (2024) The hidden network of biocrust successional stages in the High Arctic: revealing abiotic and biotic factors shaping microbial and metazoan communities. PubMed

Nagao, M., Matsui, K. and Uemura, M. (2008) PubMed

Peredo, E.L. and Cardon, Z.G. (2020) Shared up-regulation and contrasting down-regulation of gene expression distinguish desiccation-tolerant from intolerant green algae. PubMed PMC

Permann, C., Stegner, M., Roach, T., Loacker, V., Lewis, L.A., Neuner, G., et al. (2024) Striking differences in frost hardiness and inability to cold acclimate in two

Pichrtová, M., Hájek, T. and Elster, J. (2014) Osmotic stress and recovery in field populations of PubMed

Pierangelini, M., Ryšánek, D., Lang, I., Adlassnig, W. and Holzinger, A. (2017) Terrestrial adaptation of green algae Klebsormidium and Zygnema (Charophyta) involves diversity in photosynthetic traits but not in CO PubMed PMC

Přibyl, P. and Cepák, V. (2019) Screening for heterotrophy in microalgae of various taxonomic positions and potential of mixotrophy for production of high-value compounds.

Přibyl, P., Cepák, V., Kaštánek, P. and Zachleder, V. (2015) Elevated production of carotenoids by a new isolate of

Procházková, L., Remias, D., Řezanka, T. and Nedbalová, L. (2018) PubMed PMC

Pröschold, T., Marin, B., Schlösser, U.G. and Melkonian, M. (2001) Molecular phylogeny and taxonomic revision of PubMed

Pushkareva, E., Hejduková, E., Elster, J. and Becker, B. (2024) Microbial response to seasonal variation in Arctic biocrusts with a focus on fungi and cyanobacteria. PubMed

Putri, G.H., Anders, S., Pyl, P.T., Pimanda, J.E. and Zanini, F. (2022) Analysing high-throughput sequencing data in Python with HTSeq 2.0. Bioinformatics  38:2943–2945. PubMed PMC

Rindi, F. (2007) Diversity, distribution and ecology of green algae and cyanobacteria in urban habitats. In: Seckbach, J (ed) Algae and Cyanobacteria in Extreme Environments. Springer, Dordrecht, Netherlands, pp 619–638.

Rippin, M., Becker, B. and Holzinger, A. (2017) Enhanced desiccation tolerance in mature cultures of the streptophytic green alga PubMed PMC

Rippin, M., Borchhardt, N., Karsten, U. and Becker, B. (2019) Cold acclimation improves the desiccation stress resilience of polar strains of PubMed PMC

Robinson, M.D., McCarthy, D.J. and Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics  26:139–140. PubMed PMC

Rybalka, N., Blanke, M., Tzvetkova, A., Noll, A., Roos, C., Boy, J., et al. (2023) Unrecognized diversity and distribution of soil algae from Maritime Antarctica (Fildes Peninsula, King George Island). PubMed PMC

Ryšánek, D., Hrčková, K. and Škaloud, P. (2015) Global ubiquity and local endemism of free-living terrestrial protists: phylogeographic assessment of the streptophyte alga Klebsormidium. Environ. Microbiol.  17:689–698. PubMed

Ryšánek, D., Elster, J., Kováčik, L. and Škaloud, P. (2016) Diversity and dispersal capacities of a terrestrial algal genus PubMed

Seppey, M., Manni, M. and Zdobnov, E.M. (2019) BUSCO: assessing genome assembly and annotation completeness. PubMed

Silva, P.C., Mattox, K.R., Blackwell, W.H., Jr. (1972) The generic name

Škaloud, P. (2006) Variation and taxonomic significance of some morphological features in European strains of

Škaloud, P. and Rindi, F. (2013) Ecological differentiation of cryptic species within an asexual protist morphospecies: a case study of filamentous green alga PubMed

Škuta, C., Bartůněk, P. and Svozil, D. (2014) InCHlib - interactive cluster heatmap for web applications. PubMed PMC

Sluiman, H.J., Guihal, C. and Mudimu, O. (2008) Assessing phylogenetic affinities and species delimitations in Klebsormidiales (Streptophyta): nuclear-encoded rDNA phylogenies and ITS secondary structure models in PubMed

Staub, R. (1961) Ernährungsphysiologische Untersuchungen an der planktonischen Blaualge

Střížek, A., Přibyl, P., Lukeš, M., Grivalský, T., Kopecký, J., Galica, T., et al. (2023) PubMed PMC

Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. PubMed PMC

Tashyreva, D., Elster, J. and Billi, D. (2013) A novel staining protocol for multiparameter assessment of cell heterogeneity in PubMed PMC

Toca, A., Oliet, J.A., Villar-Salvador, P., Maroto, J. and Jacobs, D.F. (2018) Species ecology determines the role of nitrogen nutrition in the frost tolerance of pine seedlings. PubMed

de  Vries, J. and Archibald, J.M. (2018) Plant evolution: landmarks on the path to terrestrial life. New Phytol.  217:1428–1434. PubMed

de  Vries, J., Stanton, A., Archibald, J.M. and Gould, S.B. (2016) Streptophyte terrestrialization in light of plastid evolution. PubMed

Wang, S., Li, L., Li, H., Sahu, S.K., Wang, H., Xu, Y., et al. (2020) Genomes of early-diverging streptophyte algae shed light on plant terrestrialization. Nat Plants  6:95–106. PubMed PMC

Wickham, H. (2007) Reshaping data with the reshape package.

Wickham, H. (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York.

Wood, D.E. and Salzberg, S.L. (2014) Kraken: ultrafast metagenomic sequence classification using exact alignments. PubMed PMC

Wood, D.E., Lu, J. and Langmead, B. (2019) Improved metagenomic analysis with Kraken 2. PubMed PMC

Xu, F. and Pan, J. (2020) Potassium channel KCN11 is required for maintaining cellular osmolarity during nitrogen starvation to control proper cell physiology and TAG accumulation in PubMed PMC

Zhuo, H., Liu, X., Luo, S., Ou, X., Rong, X., Yang, L., et al. (2024) Physiological changes underlying increased photosynthetic-nitrogen use efficiency in response to low-nitrogen conditions in

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...