Non-Pigmented Antarctic Yeasts and Their Resistance to Toxic Metals

Authors

DOI:

https://doi.org/10.15407/microbiolj86.02.024

Keywords:

Antarctica, yeast, 18S rRNA, phylogenetic analysis, Leucosporidium scottii, Debaryomyces hansenii, toxic metals

Abstract

Despite the key role in biogeochemical processes and in the functioning of terrestrial ecosystems, yeasts of Antarctic regions still remain insufficiently studied. The study and analysis of the composition of Antarctic microbial communities remains relevant and is carried out using molecular biological approaches. The investigation of their resistance to toxic metal ions is essential to select industrially promising strains that can contribute to the development of new methods of metals detoxification via microorganisms. Aim. To determine the taxonomic position of non-pigmented Antarctic yeasts and investigate their resistance to toxic metal ions. Methods. The objects of the research are yeasts isolated from Antarctic phytocenoses. They were grown on malt wort (pH 5.0–5.5, temperature 18–20 °C). Isolation of genomic DNA was performed via the commercial DNA-sorb kit. Amplification of DNA was carried out using primers NL1 and NL4. Phylogenetic analysis was conducted by construction of trees (dendrograms) showing the position of the studied strains among closely related and typical species. The resistance of yeasts to toxic metal ions was established by cultivation in the concentration gradient of Ni2+, Co2+, CrO42-, and Сu2+. The ecophysiological traits of the isolated yeast strains including psychro- and halotolerance were determined. Results. Phylogenetic analysis showed a high percentage of similarity (99.5–99.6 %) of sequences of 18S rRNA genes of Antarctic yeast strains with the yeast sequences from the GenBank database. Psychrotolerant and halotolerant Antarctic yeast strains S11 and S12 were identified as Leucosporidium scottii and Debaryomyces hansenii, respectively. The studied yeast strains were found to be the most resistant to metal ions Ni2+ and Co2+. Strain of L. scottii S11 grew at 800 mg/L of Co2+, and D. hansenii S12 – at 750 mg/L of Ni2+. The yeasts were the least resistant to CrO42-: the L. scottii S11 and D. hansenii S12 strains grew at concentrations of 25 mg/L and 150 mg/L, respectively. In the presence of Cu2+, they grew at the same concentration – 600 mg/L. The combined action of toxic metal ions resulted in the increased toxic effects on the studied yeasts. Conclusions. The nucleotide sequences of 18S rRNA gene fragment of yeast strains S11 and S12 were included in the GenBank database under the numbers LT220858 and LT220859. Metal-resistant psychrotolerant yeast strains can be used to evaluate the metals content in polar regions as well as to bioremediate metal-contaminated ecosystems. However, further research is needed to develop and optimize bioremediation processes.

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References

Białkowska, A. M., Szulczewska, K. M., Krysiak, J., Florczak, T., Gromek, E., Kassassir, H., et al. (2017). Genetic and biochemical characterization of yeasts isolated from Antarctic soil samples. Polar Biology, 40, 1787-1803. https://doi.org/10.1007/s00300-017-2102-7

Brandao, L. R., Vaz, A. B. M., Santo, L. C. E., Pimenta, R. S., Morais, P. B., Libkind, D., et al. (2017). Diversity and biogeographical patterns of yeast communities in Antarctic, Patagonian and tropical lakes. Fungal Ecology, 28, 33-43. https://doi.org/10.1016/j.funeco.2017.04.003

Brandao, R. L., Libkind, D., Vaz, B. M. A., Santo, L. C. E., Moliné, M., de García, V., et al. (2011). Yeasts from an oligotrophic lake in Patagonia (Argentina): diversity, distribution and synthesis of photoprotective compounds and extracellular enzymes. FEMS Microbiology Ecology, 76(1), 1-13. https://doi.org/10.1111/j.1574-6941.2010.01030.x

Buzzini, P., Branda, E., Goretti, M., & Turchetti, B. (2012). Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiology Ecology, 82, 217-241. https://doi.org/10.1111/j.1574-6941.2012.01348.x

Carrasco, М., Rozas, J. M., Barahona, S., Alcaíno, J., Cifuentes, V., & Baeza, M. (2012). Diversity and extracellular enzymatic activities of yeasts isolated from King George Island, the sub-Antarctic region. BMC Microbiology, 12, 251. doi: 10.1186/1471-2180-12-251 https://doi.org/10.1186/1471-2180-12-251

Cervantes, C., Campos-García, J., Devars, S., Gutiérrez-Corona, F., Loza-Tavera, H., Torres-Guzmán, J. C., et al. (2001). Interactions of chromium with microorganisms and plants. FEMS Microbiology Reviews, 25(3), 335-347. https://doi.org/10.1111/j.1574-6976.2001.tb00581.x

Corsolini, S. (2009). Industrial contaminants in Antarctic biota. Journal of Chromatography A, 1216, 598-612. https://doi.org/10.1016/j.chroma.2008.08.012

Cruz, E. L., Pajot, H. F., Martorell, M. M., Cormack, W. P. M., de Figueroa, L. I. C. & Fernández, P. M. (2022). Isolated indigenous yeasts from Antarctica with the ability to remove toxic hexavalent chromium. Journal of Chemical Ecology, 38(7), 1-18. https://doi.org/10.1080/02757540.2022.2066084

Degen, O., & Eitinger, T. (2002). Substrate specificity of nickel/cobalt permeases: insights from mutants altered in transmembrane domains I and II. Journal of Bacteriology, 184(13), 3569-3577. https://doi.org/10.1128/JB.184.13.3569-3577.2002

Duarte, A. W. F., Dayo-Owoyemi, I., Nobre, F. S., Pagnocca, F. C, Chaud, L. C. S., Pessoa, A., et al. (2013). Taxonomic assessment and enzymes production by yeasts isolated from marine and terrestrial Antarctic samples. Extremophiles, 17, 1023-1035. https://doi.org/10.1007/s00792-013-0584-y

Elabed, A., Ezziat, L., Ibnsouda, S., Elabed, S., & Erable, B. (2021). Bioelectrochemical сharacterization of heavy metals resistant yeast: hansenula fabianii isolated from tannery wastewater. International Journal of Electrochemical Science, 16(1), 140128. https://doi.org/10.20964/2021.01.31

Fernandez, P. M., Martorell, M. M., Blaser, M. G., Ruberto, L. A. M., de Figueroa, L. I. C. & Cormack, W. P. M. (2017). Phenol degradation and heavy metal tolerance of Antarctic yeasts. Extremophiles, 21, 445-457. https://doi.org/10.1007/s00792-017-0915-5

Forzani, C., Loulergue, C., Lobréaux, S., Briat, J. F., & Lebrun, M. (2001). Nickel resistance and in condensation in Saccharomyces cerevisiae expressing a maize high mobility group I/Y protein. Journal of Biological Chemistry, 276(20), 16731-16738. https://doi.org/10.1074/jbc.M007462200

George, P. L., Sripathi, V. R., Nyaku, S. T., & Sharma, G. C. (2016). DNA-based identification of Lentinula edodes strains with species-specific primers. African Journal of Biotechnology, 15(7), 191-198. https://doi.org/10.5897/AJB2015.15089

Godinho, V. M., Furbino, L. E., Santiago, I. F., Pellizzari, F. M., Yokoya, N. S., Pupo, D., et al. (2013). Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. International Society for Microbial Microbiology, 7, 1434-1451. https://doi.org/10.1038/ismej.2013.77

Gomes, E. C. Q, Figueredo, H. M., de Oliveira, F. S., Schaefer, C. E. G. R., Michel, R. F., Rosa, C.A., et al. (2019). Fungi present in soils of Antarctica. Fungi of Antarctica. Springer, Cham, 43-67. https://doi.org/10.1007/978-3-030-18367-7_3

Gumá-Cintrón, Y., Bandyopadhyay, A., Rosado, W., Shu-Hu, W., & Nadathur, G. S. (2015). Transcriptomic analysis of cobalt stress in the marine yeast Debaryomyces hansenii. FEMS Yeast Research, 15(8):fov099. https://doi.org/10.1093/femsyr/fov099

Gupta, A., Gupta, R., & Singh, R. L. (2017). Microbes and environment. Principles and Applications of Environmental Biotechnology for a Sustainable Fut, 43-84. https://doi.org/10.1007/978-981-10-1866-4_3

Gupta, R., Kumari, A., Syal, P., & Singh, Y. (2015). Molecular and functional diversity of yeast and fungal lipases: their role in biotechnology and cellular physiology. Progress in Lipid Research, 57, 40-54. https://doi.org/10.1016/j.plipres.2014.12.001

Havryliuk, O., Hovorukha, V., & Tashyrev, O. (2018). The resistance of chernozem soil microorganisms to soluble copper compounds. Faktori Eksperimentalʹnoï Evolûcìï Organìzmìv, 23, 273-279. https://doi.org/10.7124/FEEO.v23.1027

Hebel, I., Galleguillos, C., Jana, R., & Dacasa-Rudinger, M. D. C. (2012). Early knowledge of Antarctica's vegetation: expanding past and current evidence. Revista Chilena De Historia Natural, 85, 409-418. https://doi.org/10.4067/S0716-078X2012000400004

Kachalkin, A. V., Glushakova, A. M., Yurkov, A. M., & Chernov, I. Yu. (2008). Characterization of yeast groupings in the phyllosphere of Sphagnum mosses. Mikrbiologiya, 77(2), 474-481. https://doi.org/10.1134/S0026261708040140

Kan, G., Wang, X., Jiang, J., Zhang, C., Chi, M., Ju, Y., et al. (2019). Copper stress response in yeast Rhodotorula mucilaginosa AN5 isolated from sea ice, Antarctic. Microbiologyopen, 8, e657. https://doi.org/10.1002/mbo3.657

Margesin, R., & Miteva, V. (2011). Diversity and ecology of psychrophilic microorganisms. Research in Microbiology, 162, 346-361. https://doi.org/10.1016/j.resmic.2010.12.004

Martinez, A., Cavello, I., Garmendia, G., Rufo, C., Cavalitto, S., & Vero, S. (2016). Yeasts from sub-Antarctic region: biodiversity, enzymatic activities and their potential as oleaginous microorganisms. Extremophiles, 20, 759-769. https://doi.org/10.1007/s00792-016-0865-3

de Menezes, G. C., Amorim, S. S., Gonçalves, V. N., Godinho, V. M., Simões, J. C., Rosa, C. A., еt al. (2019). Diversity, distribution, and ecology of fungi in the seasonal snow of Antarctica. Microorganisms, 7(10), 445. https://doi.org/10.3390/microorganisms7100445

Moreno, A., Demitri, N., Ruiz-Baca, E., Vega-González, A., Polentarutti, M., & Cuéllar-Cruz, M. (2019). Bioreduction of precious and heavy metals by Candida species under oxidative stress conditions. Microbial Biotechnology, 12(6), 1164-1179. https://doi.org/10.1111/1751-7915.13364

Nagahama, T. (2006). Yeast biodiversity in freshwater, marine and deep-sea environments. Springer-Verlag, Berlin, 241-262. https://doi.org/10.1007/3-540-30985-3_12

Podgorskiĭ, V. S., & Kasatkina, T. P. (2003). Yeasts - biosorbents of heavy metals. Microbiological Journal, 66(1), 91-103.

Poli, A., Anzelmo, G., Tommonaro, G., Pavlova, K., Casaburi, A. & Nicolaus, B. (2010). Production and chemical characterization of anexopolysaccharide synthesized by psychrophilic yeast strain Sporobolomyces salmonicolor AL1 isolated from Livingston Island, Antarctica. Folia Microbiologica, 55, 576-581. https://doi.org/10.1007/s12223-010-0092-8

Rajpert, L., Skłodowska, A., & Matlakowska, R. (2013). Biotransformation of copper from Kupferschiefer black shale (Fore-Sudetic Monocline, Poland) by yeast Rhodotorula mucilaginosa LM9. Chemosphere, 91, 1257-1265. https://doi.org/10.1016/j.chemosphere.2013.02.022

Ram, C. B., Nelly, G., & Nevena, L. (2012). Bioremediation of chromium ions with filamentous yeast Trichosporon cutaneum R57. Jornal of Biology and Earth Sciences, 2, 70-75.

Rehman, M., Liu, L., Wang, Q., Saleem, M. H., Bashir, S., Ullah, S., et al. (2019). Copper environmental toxicology, recent advances, and future outlook: a review. Environmental Science and Pollution Research, 26(18), 18003-18016. https://doi.org/10.1007/s11356-019-05073-6

Robinson, S. A., Wasley, J., & Tobin, A. K. (2003). Living on the edge-plants and global change in continental and maritime Antarctica. Global Change Biology, 9, 1681-1717. https://doi.org/10.1046/j.1365-2486.2003.00693.x

Rodionov, D. A., Hebbeln, P., Gelfand, M. S., & Eitinger, T. (2006). Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: Evidence for a novel group of ATP-Binding cassette transporters. Journal of Bacteriology, 188(1), 317-327. https://doi.org/10.1128/JB.188.1.317-327.2006

Rosa, L. H., Zani, C. L., Cantrell, C. L., Duke, S. O., Dijck, P. V., Desideri, A., еt al. (2019). Fungi in Antarctica: diversity, ecology, effects of climate change, and bioprospecti on for bioactive compounds. Fungi of Antarctica. Springer, Cham, 1-17. https://doi.org/10.1007/978-3-030-18367-7_1

Sampaio, A. C., Bezerra, R. M. F., & Dias, A. A. (2018). Mediterranean forested wetlands are yeast hotspots for bioremediation: a case study using azo dyes. Scientific Reports, 8, 15943. https://doi.org/10.1038/s41598-018-34325-7

Sampaio, J. P., Agerer, R., Piepenbring, M., & Blanz, P. (2004). Diversity, phylogeny and classification of basidiomycetous yeasts. Frontiers in Basidiomycote Mycology. IHW Verlag, Eching, 49-80.

Santiago, I. F., Soares, M. A., Rosa, C. A., & Rosa, L. H. (2015). Lichensphere: A protected natural microhabitat of the non-lichenised fungal communities living in extreme environments of Antarctica. Extremophiles, 19, 1087-1097. https://doi.org/10.1007/s00792-015-0781-y

Savastru, E., Bulgariu, D., Zamfir, C-I., & Bulgariu, L. (2022). Application of Saccharomyces cerevisiae in the biosorption of Co(II), Zn(II) and Cu(II) іons from аqueous media. Water, 14(6), 976. https://doi.org/10.3390/w14060976

Schultz, J., & Rosado, A. S. (2019). Microbial role in the ecology of Antarctic plants. In: The ecological role of microorganisms in the Antarctic environment. Springer Polar Sciences, 257-275. https://doi.org/10.1007/978-3-030-02786-5_12

Sharma, P., Singh, S. P., Parakh, S. K., & Tong, Y. W. (2022). Health hazards of hexavalent chromium (Cr (VI)) and its microbial reduction. Bioengineered, 13(3), 4923-4938. https://doi.org/10.1080/21655979.2022.2037273

Silver, S., & Phung, L. T. (2005). A bacterial view of the periodic table: genes and proteins for toxic in organic ions. Journal of Industrial Microbiology and Biotechnology, 32, 587-605. https://doi.org/10.1007/s10295-005-0019-6

Singh, J., Singh, R. P., & Khare, R. (2018). Influence of climate change on Antarctic flora. Polar Science, 18, 94-101. https://doi.org/10.1016/j.polar.2018.05.006

Sodhi, K. K., Kumar, M., & Singh, D. K. (2020). Multi metal resistance and potential of Alcaligenes sp. MMA for the removal of heavy metals. SN Applied Sciences, 2, 1885. https://doi.org/10.1007/s42452-020-03583-4

Tian, Y., Li, Y. L., & Zhao, F. C. (2017). Secondary metabolites from polar organisms. Marine Drugs, 15, E28. https://doi.org/10.3390/md15030028

Tomova, I., Stoilova-Disheva, M., Lazarkevich, I., & Vasileva-Tonkova, E. (2015). Antimicrobial activity and resistance to heavy metals and antibiotics of heterotrophic bacteria isolated from sediment and soil samples collected from two Antarctic islands. Frontiers in Life Science, 8(4), 348-357. https://doi.org/10.1080/21553769.2015.1044130

Turkiewicz, M., Pazgier, M., Kalinowska, H., & Bielecki, S. (2003). A cold adapted extracellular serine proteinase of the yeast Leucosporidium antarcticum. Extremophiles, 7(3), 435-442. https://doi.org/10.1007/s00792-003-0340-9

Vadkertiová, R., & Sláviková, E. (2006). Metal tolerance of yeasts isolated from water, soil and plant environments. Journal of Basic Microbiology, 46(2), 145-52. https://doi.org/10.1002/jobm.200510609

Vasileva-Tonkova, E., Romanovskaya, V., Gladka, G., Gouliamova, D., Tomova, I., Stoilova-Disheva, M., & Tashyrev, O. (2014). Ecophysiological properties of cultivable heterotrophic bacteria and yeasts dominating in phytocenoses of Galindez Island, maritime Antarctica. World Journal of Microbiology and Biotechnology, 30(4), 1387-1398. https://doi.org/10.1007/s11274-013-1555-2

Zhang, T., Zhang, Y. Q., Liu, H. Y., Wei, Y. Z., Li, H. L., Su, J., et al. (2013). Diversity and cold adaptation of culturable endophytic fungi from bryophytes in the Fildes Region, King George Island, maritime Antarctica. FEMS Microbiology Letters, 341(1), 52-61. https://doi.org/10.1111/1574-6968.12090

Zibilski, L. M., & Wagnar, G. H. (1982). Bacterial growth and fungal genera distribution in soil amended with sewage sluge containing cadmium, chromium and copper. Soil Science, 134(6), 364-369. https://doi.org/10.1097/00010694-198212000-00004

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Published

2024-04-28

How to Cite

Gladka, G., Hovorukha, V., Havryliuk О., Bida, I., Yastremska, L., & Tashyrev, O. (2024). Non-Pigmented Antarctic Yeasts and Their Resistance to Toxic Metals. Mikrobiolohichnyi Zhurnal, 86(2), 24-35. https://doi.org/10.15407/microbiolj86.02.024
Received 2023-06-20
Accepted 2023-10-25
Published 2024-04-28