Ukrainian Antarctic Journal

Vol 22 No 1(28) (2024): Ukrainian Antarctic Journal
Articles

Plant growth-promoting potential of bacterial isolates from the rhizosphere of Deschampsia antarctica

PDF
  • Olga Maslovska,
  • Solomiia Komplikevych,
  • Iryna Danylo,
  • Ivan Parnikoza,
  • Svitlana Hnatush
Olga Maslovska
Ivan Franko National University of Lviv, Lviv, 79005, Ukraine
Solomiia Komplikevych
Ivan Franko National University of Lviv, Lviv, 79005, Ukraine
Iryna Danylo
Ivan Franko National University of Lviv, Lviv, 79005, Ukraine
Ivan Parnikoza
State Institution National Antarctic Scientific Center, Ministry of Education and Science of Ukraine, Kyiv, 01601, Ukraine; Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, Kyiv, 03143, Ukraine
Svitlana Hnatush
Ivan Franko National University of Lviv, Lviv, 79005, Ukraine
DOI: https://doi.org/10.33275/1727-7485.1.2024.728
Published September 7, 2024
Keywords
  • auxin-like substances,
  • Bacillus,
  • microbiota of the rhizosphere,
  • phosphorus solubilization,
  • plant growth-promoting bacteria,
  • siderophores
    • ...More
    Less
How to Cite
Maslovska, O., Komplikevych, S., Danylo, I., Parnikoza, I., & Hnatush, S. (2024). Plant growth-promoting potential of bacterial isolates from the rhizosphere of Deschampsia antarctica. Ukrainian Antarctic Journal, 22(1(28), 63-81. https://doi.org/10.33275/1727-7485.1.2024.728

Copyright (c) 2024 Ukrainian Antarctic Journal

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Abstract

Plants’ adaptations, in combination with the rhizosphere and endosphere microbiome, ensure their survival in the extreme conditions of the Antarctic. The work aimed to quantify the culturable microorganisms of different groups and establish the plant growth-promoting potential of bacterial isolates from the rhizosphere of Deschampsia antarctica. Standard microbiological methods (enumeration of microorganisms and study of the properties of isolates, in particular, the cell wall organization by Gram staining, motility, endospore formation, growth at different temperatures, halotolerance, need for oxygen, ability to assimilate some organic carbon sources) and biochemical methods to determine the properties of isolates (oxidase, catalase activities, tests for the ability to reduce nitrate, produce amylases, lipases, proteases). The ability of the isolates to produce siderophores was determined using a medium with chromazurol S and hexadecyltrimethylammonium bromide, to solubilize insoluble phosphate-containing compounds using Pikowska’s medium with Ca3(PO4)2 and Menkina’s medium with egg lecithin. The content of auxin-like substances in the medium was determined by the Salkowski method. The effect of the isolates on wheat growth was determined by the germination of wheat seeds treated with the isolates, the length of shoots and roots of plants, and chlorophyll content in leaves. The isolates were identified using phylogenetic analysis of the 16S rRNA gene. The most abundant groups of microorganisms in the rhizosphere of D. antarctica were oligotrophic, oligonitrophilic, and cellulose-degrading microorganisms. Among 120 isolates of the rhizosphere zone of D. antarctica, 7 oligonitrophilic isolates (RE1, RE3, RE4, RE8, RP8, RO4, RT1) were selected, which solubilized insoluble phosphate-containing compounds, synthesized lipases, amylases, auxin-like substances, and siderophores. Isolate RT1 (Bacillus sp. RT1 by physiological and biochemical properties and the 16S rRNA gene) showed the best plant growth-promoting properties. Treatment of wheat seeds with this isolate increased germination by 25%, shoot and root length by 15%, leaf area 3 times, and chlorophyll content 1.6 times.

PDF

References

  1. Acuña-Rodríguez, I. S., Hansen, H., Gallardo-Cerda, J., Atala, C., & Molina-Montenegro, M. A. (2019). Antarctic extremophiles: biotechnological alternative to crop productivity in saline soils. Frontiers in Bioengineering and Biotechnology, 7. https://doi.org/10.3389/fbioe.2019.00022
  2. Adiguzel, A., Ay, H., Baltaci, M. O., Akbulut, S., Albayrak, S., & Omeroglu, M. A. (2020). Genome-based classification of Calidifontibacillus erzurumensis gen. nov., sp. nov., isolated from a hot spring in Turkey, with re-classification of Bacillus azotoformans as Calidifontibacillus azotoformans comb. nov. and Bacillus oryziterrae as Calidifontibacillus oryziterrae comb. nov. International Journal of Systematic and Evolutionary Microbiology, 70(12), 6418–6427. https://doi.org/10.1099/ijsem.0.004549
  3. Ahmed, S., Rahman, M. S., Hasan, M. M., Paul, N., & Sajib, A. A. (2018). Microbial degradation of lignocellulosic biomass: discovery of novel natural lignocellulolytic bacteria. BioTechnologia, 99(2), 137–146. https://doi.org/10.5114/bta.2018.75657
  4. Bertini, L., Proietti, S., Fongaro, B., Holfeld, A., Picotti, P., Falconieri, G. S., Bizzarri, E., Capaldi, G., Polverino de Laureto, P., & Caruso, C. (2022). Environmental signals act as a driving force for metabolic and defense responses in the Antarctic plant Colobanthus quitensis. Plants, 11(22), 3176. https://doi.org/10.3390/plants11223176
  5. Di Benedetto, N. A, Corbo, M. R., Campaniello, D., Cataldi, M. P., Bevilacqua, A., Sinigaglia, M., & Flagella, Z. (2017). The role of Plant Growth Promoting Bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat. AIMS Microbiology, 3(3), 413–434. https://doi.org/10.3934/microbiol.2017.3.413
  6. Gallardo-Cerda, J., Levihuan, J., Lavín, P., Oses, R., Atala, C., Torres-Díaz, C., Cuba-Díaz, M., Barrera, A., & Molina-Montenegro, M. A. (2018). Antarctic rhizobacteria improve salt tolerance and physiological performance of the Antarctic vascular plants. Polar Biology, 41(10), 1973–1982. https://doi.org/10.1007/s00300-018-2336-z
  7. Gang, S., Sharma, S., Saraf, M., Buck, M., & Schumacher, J. (2019). Analysis of indole-3-acetic acid (IAA) production in Klebsiella by LC-MS/MS and the Salkowski method. BIO-PROTOCOL, 9(9), e3230. https://doi.org/10.21769/bioprotoc.3230
  8. Garcia, J., Schmidt, J. E., Gidekel, M., & Gaudin, A. C. M. (2021). Impact of an antarctic rhizobacterium on root traits and productivity of soybean (Glycine max L.). Journal of Plant Nutrition, 44(12), 1818–1825. https://doi.org/10.1080/01904167.2021.1884704
  9. Glick, B. R., & Pasternak, J. J. (2003). Plant growth promoting bacteria. Molecular biotechnology: principles and applications of recombinant DNA (p. 436–454). Washington DC, ASM Press.
  10. Green, M. R., & Sambrook, J. (2012). Molecular Cloning: A Laboratory Manual (4th ed.). Cold Spring Harbor Laboratory Press.
  11. Grzesiak, J., Kaczyńska, A., Gawor, J., Żuchniewicz, K., Aleksandrzak-Piekarczyk, T., Gromadka, R., & Zdanowski, M. K. (2020). A smelly business: Microbiology of Adélie penguin guano (Point Thomas rookery, Antarctica). Science of The Total Environment, 714, 136714. https://doi.org/10.1016/j.scitotenv.2020.136714
  12. Guajardo-Leiva, S., Alarcón, J., Gutzwiller, F., Gallardo-Cerda, J., Acuña-Rodríguez, I. S., Molina-Montenegro, M., Crandall, K. A., Pérez-Losada, M., & Castro-Nallar, E. (2022). Source and acquisition of rhizosphere microbes in Antarctic vascular plants. Frontiers in Microbiology, 13. https://doi.org/10.3389/fmicb.2022.916210
  13. Han, P., Tang, X., Koch, H., Dong, X., Hou, L., Wang, D., Zhao, Q., Li, Z., Liu, M., Lücker, S., & Shi, G. (2024). Unveiling unique microbial nitrogen cycling and nitrification driver in coastal Antarctica. Nature Communications, 15(1), 3143. https://doi.org/10.1038/s41467-024-47392-4
  14. Hayat, R., Ali, S., Amara, U., Khalid, R., & Ahmed, I. (2010). Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology, 60, 579–598. https://doi.org/10.1007/s13213-010-0117-1
  15. Hudz’, S. P., Hnatush, S. O., Yavorska, H. V., Bilinska, I. S., & Borsukevych, B. M. (2014). Guidebook on microbiology. Publishing centre at Ivan Franko Lviv National University, Lviv. (In Ukrainian)
  16. Hwangbo, K., Um, Y., Kim, K. Y., Madhaiyan, M., Sa, T. M., & Lee, Y. (2016). Complete genome sequence of Bacillus velezensis CBMB205, a phosphate-solubilizing bacterium isolated from the rhizoplane of rice in the Republic of Korea. Genome Announcements, 4(4). https://doi.org/10.1128/genomea.00654-16
  17. Kim, O.-S., Chae, N., Lim, H. S., Cho, A., Kim, J. H., Hong, S. G., & Oh, J. (2012). Bacterial diversity in ornithogenic soils compared to mineral soils on King George Island, Antarctica. Journal of Microbiology, 50(6), 1081–1085. https://doi.org/10.1007/s12275-012-2655-7
  18. Khan, N., Bano, A., & Babar, M. A. (2019). Metabolic and physiological changes induced by plant growth regulators and plant growth promoting rhizobacteria and their impact on drought tolerance in Cicer arietinum L. PLOS ONE, 14(3), e0213040. https://doi.org/10.1371/journal.pone.0213040
  19. Komplikevych, S., Maslovska, O., Peretyatko, T., Moroz, O., Diakiv, S., Zaritska, Y., Parnikoza, I., & Hnatush, S. (2023). Culturable microorganisms of substrates of terrestrial plant communities of the maritime Antarctic (Galindez Island, Booth Island). Polar Biology, 46(1), 1–19. https://doi.org/10.1007/s00300-022-03103-7
  20. Kozeretska, I. A., Parnikoza, I. Yu., Mustafa, O., Tyschenko, O. V., Korsun, S. G., & Convey, P. (2010). Development of Antarctic herb tundra vegetation near Arctowski station, King George Island. Polar Science, 3(4), 254–261. https://doi.org/10.1016/j.polar.2009.10.001
  21. Kramer, J., Özkaya, Ö., & Kümmerli, R. (2020). Bacterial siderophores in community and host interactions. Nature Reviews Microbiology, 18(3), 152–163. https://doi.org/10.1038/s41579-019-0284-4
  22. Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
  23. Lo Giudice, A., Michaud, L., De Pascale, D., De Domenico, M., Di Prisco, G., Fani, R., & Bruni, V. (2006). Lipolytic activity of Antarctic cold-adapted marine bacteria (Terra Nova Bay, Ross Sea). Journal of Applied Microbiology, 101(5), 1039–1048. https://doi.org/10.1111/j.1365-2672.2006.03006.x
  24. Loperena, L., Soria, V., Varela, H., Lupo, S., Bergalli, A., Guigou, M., Pellegrino, A., Bernardo, A., Calviño, A., Rivas, F., & Batista, S. (2012). Extracellular enzymes produced by microorganisms isolated from maritime Antarctica. World Journal of Microbiology and Biotechnology, 28(5), 2249–2256. https://doi.org/10.1007/s11274-012-1032-3
  25. Louden, B. C., Haarmann, D., & Lynne, A. M. (2011). Use of blue agar CAS assay for siderophore detection. Journal of Microbiology & Biology Education, 12(1), 51–53. https://doi.org/10.1128/jmbe.v12i1.249
  26. Madhaiyan, M., Poonguzhali, S., Kwon, S.-W., & Sa, T.-M. (2010). Bacillus methylotrophicus sp. nov., a methanol-utilizing, plant-growth-promoting bacterium isolated from rice rhizosphere soil. International Journal of Systematic and Evolutionary Microbiology, 60(10), 2490–2495. https://doi.org/10.1099/ijs.0.015487-0
  27. Merck. (2005). Merck Microbiology Manual, 12th ed. Merck, Darmstadt, Germany.
  28. Molina-Montenegro, M. A., Acuña-Rodríguez, I. S., Torres-Díaz, C., Gundel, P. E., & Dreyer, I. (2020). Antarctic root endophytes improve physiological performance and yield in crops under salt stress by enhanced energy production and Na+ sequestration. Scientific Reports, 10(1), 5819. https://doi.org/10.1038/s41598-020-62544-4
  29. Nautiyal, C. S. (1999). An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiology Letters, 170(1), 265–270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
  30. Nei, M., & Kumar, S. (2000). Molecular evolution and phylogenetics. Oxford University Press.
  31. Olanrewaju, O. S., Glick, B. R., & Babalola, O. O. (2017). Mechanisms of action of plant growth promoting bacteria. World Journal of Microbiology and Biotechnology, 33(11), 197. https://doi.org/10.1007/s11274-017-2364-9
  32. Ozheredova, I. P., Parnikoza, I. Yu., Poronnik, O. O., Kozeretska, I. A., Demidov, S. V., & Kunakh, V. A. (2015). Mechanisms of antarctic vascular plant adaptation to abiotic environmental factors. Cytology and Genetics, 49(2), 139-145. https://doi.org/10.3103/s0095452715020085
  33. Pandey, S. S., Singh, P., Samal, B., Verma, R. K., & Chatterjee, S. (2017). Xanthoferrin siderophore estimation from the cell-free culture supernatants of different Xanthomonas strains by HPLC. BIO-PROTOCOL, 7(14), e2410. https://doi.org/10.21769/bioprotoc.2410
  34. Persello-Cartieaux, F., Nussaume, L., & Robaglia, C. (2003). Tales from the underground: molecular plant–rhizobacteria interactions. Plant, Cell & Environment, 26(2), 189–199. https://doi.org/10.1046/j.1365-3040.2003.00956.x
  35. Petrovska, I. R., Salyga, Y. T., & Vudmaska, I. V. (2022). Statistical methods in biological research: a textbook. Agrarian Science. (In Ukrainian)
  36. Prekrasna, I., Pavlovska, M., Miryuta, N., Dzhulai, A., Dykyi, E., Convey, P., Kozeretska, I., Bedernichek, T., & Parnikoza, I. (2022). Antarctic hairgrass rhizosphere microbiomes: microscale effects shape diversity, structure, and function. Microbes and Environments, 37(2), ME21069. https://doi.org/10.1264/jsme2.me21069
  37. Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology, 17(1), 208–212. https://doi.org/10.1083/jcb.17.1.208
  38. Roman, 2., & Gromyko, O. (2023). Plant growth promoting properties of an antarctic strain Amycolatopsis sp. Cq 72-27. Ukrainian Antarctic Journal, 21 (1(26)), 79–89. https://doi.org/10.33275/1727-7485.1.2023.708
  39. Romaniuk, N. D., Tsvilynyuk, O. M., Mykyievych, I. M., & Terek, O. I. (2005). Guidebook on plant physiology. Lviv: Ivan Franko National University of Lviv. (In Ukrainian)
  40. Styczynski, M., Biegniewski, G., Decewicz, P., Rewerski, B., Debiec-Andrzejewska, K., & Dziewit, L. (2022). Application of psychrotolerant Antarctic bacteria and their metabolites as efficient plant growth promoting agents. Frontiers in Bioengineering and Biotechnology, 10, 772891. https://doi.org/10.3389/fbioe.2022.772891
  41. Tamura, K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Molecular Biology and Evolution, 9, 678–687.
  42. Teixeira, L. C. R. S., Peixoto, R. S., Cury, J. C., Sul, W. J., Pellizari, V. H., Tiedje, J., & Rosado, A. S. (2010). Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. The ISME Journal, 4(8), 989–1001. https://doi.org/10.1038/ismej.2010.35
  43. Teixeira, L. C. R. S., Peixoto, R. S., & Rosado, A. S. (2013). Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay in maritime Antarctica. In de Bruijn, F. J. (Ed.), Molecular Microbial Ecology of the Rhizosphere (pp. 1105–1112). John Wiley & Sons, Inc. https://doi.org/10.1002/9781118297674.ch105
  44. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673–4680. https://doi.org/10.1093/nar/22.22.4673
  45. Turner, S., Pryer, K. M., Miao, V. P. W., & Palmer, J. D. (1999). Investigating deep phylogenetic relationships among Cyanobacteria and plastids by small subunit rRNA sequence analysis. The Journal of Eukaryotic Microbiology, 46(4), 327–338. https://doi.org/10.1111/j.1550-7408.1999.tb04612.x
  46. Vijayalakshmi, Sushma, K., Abha, S., & Chander, P. (2012). Isolation and characterization of Bacillus subtilis KC3 for amylolytic activity. International Journal of Bioscience, Biochemistry and Bioinformatics, 2(5), 336–341 https://doi.org/10.7763/ijbbb.2012.v2.128
  47. Yerkhova, A., Parnikoza, I., Pavlovska, M., Yevchun, H., & Prekrasna-Kviatkovska, Y. (2022). Microbiomes of Antarctic pearlwort (Colobanthus quitensis) of the maritime Antarctic: distinct diversity and core microbes in rhizosphere and endosphere compartments of the plant. Ukrainian Antarctic Journal, 20(2(25)), 212–240. https://doi.org/10.33275/1727-7485.2.2022.701
  48. Znój, A., Gawor, J., Gromadka, R., Chwedorzewska, K. J., & Grzesiak, J. (2021). Root-associated bacteria community characteristics of Antarctic plants: Deschampsia antarctica and Colobanthus quitensis – a comparison. Microbial Ecology, 84(3), 808–820. https://doi.org/10.1007/s00248-021-01891-9
  49. Znój, A., Grzesiak, J., Gawor, J., Gromadka, R., & Chwedorzewska, K. J. (2022). Highly specialized bacterial communities within three distinct rhizocompartments of Antarctic hairgrass (Deschampsia antarctica Desv.). Polar Biology, 45(5), 833–844. https://doi.org/10.1007/s00300-022-03027-2