Effect of Different Metals on Synthesis of Siderophores by Endophyte Bacteria Isolated from Various Annual Plants

Year 2024, Volume: 34 Issue: 3, 406 - 416, 30.09.2024

Şilan Atbaş Bilgin Taşkın

https://doi.org/10.29133/yyutbd.1427459

Abstract

Endophyte bacteria are microorganisms that pass all or part of their life cycle in the tissues of healthy plants without causing any obvious signs of disease. Most siderophore-producing endophytic bacteria could improve the plant growth. Here, the effect of metals, iron (Fe), nickel (Ni), and cobalt (Co), on the growth and siderophore production profiles of 30 endophyte bacterial isolates were investigated. The results of the Minimum Inhibition Concentration (MIC) tests showed that endophytes exhibit varying degrees of tolerance to heavy metals and the metal tolerance decreased in the order Fe3+>Ni2+>Co2+. It was revealed that while 10 isolates could not produce siderophores under any circumstances, 20 isolates produced siderophores at different degrees, and siderophore molecules synthesized and secreted by these 20 isolates had affinities for all three metals (Fe3+, Co2+, and Ni2+). In addition, siderophore production profiles of isolates under each heavy metal stress were investigated by adding these metals to the Chromium Azurol Sulfonate (CAS) medium at optimum concentration. The results suggested that siderophore synthesis could be one of the coping mechanisms of only two isolates with Co2+ and Ni2+ heavy metals. In the final stage of the study, molecular identification of a certain number of isolates selected according to their siderophore production values was carried out by 16S rRNA sequencing. As a result of the sequence analysis, 2 Pseudomonas sp., 4 Bacillus sp., 1 Chryseobacterium sp., 1 Staphylococcus sp., and 1 Peribacillus sp. were revealed.

Keywords

Siderophore, Heavy Metal, Endohyte

Supporting Institution

The Scientific Research Project Units of Van Yuzuncu Yil University

Project Number

FYL-2019-8770

Thanks

This work was supported by the Scientific Research Project Units of Van Yuzuncu Yil University, Turkey (Project number: FYL-2019-8770). Also we sincerely thank Assoc. Prof. Dr. Ahmet Akkopru, Van Yuzuncu Yil University, Turkey for his support.

References

• Afzal, I., Shinwari, Z. K., Sikandar, S., & Shahzad, S. (2019). Plant beneficial endophytic bacteria: Mechanisms, diversity, host range and genetic determinants. Microbiological Research, 221, 36–49. https://doi.org/10.1016/j.micres.2019.02.001
• Arora, N. K., & Verma, M. (2017). Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech, 7(6), 381. https://doi.org/10.1007/s13205-017-1008-y
• Braud, A., Jézéquel, K., Bazot, S., & Lebeau, T. (2009). Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere, 74(2), 280–286. https://doi.org/10.1016/j.chemosphere.2008.09.013
• Cabaj, A., & Kosakowska, A. (2009). Iron-dependent growth of and siderophore production by two heterotrophic bacteria isolated from brackish water of the southern Baltic Sea. Microbiological Research, 164(5), 570–577. https://doi.org/10.1016/j.micres.2007.07.001
• Carrim, A. J. I., Barbosa, E. C., & Vieira, J. D. G. (2006). Enzymatic activity of endophytic bacterial isolates of Jacaranda decurrens Cham.(Carobinha-do-campo). Brazilian Archives of Biology and Technology, 49, 353-359. https://doi.org/10.1590/S1516-89132006000400001
• Dogan, G., & Taskin, B. (2021). Hydrolytic Enzymes Producing Bacterial Endophytes of Some Poaceae Plants. Polish Journal of Microbiology, 70(3), 297–304. https://doi.org/10.33073/pjm-2021-026
• Edberg, F., Kalinowski, B. E., Holmström, S. J., & Holm, K. (2010). Mobilization of metals from uranium mine waste: the role of pyoverdines produced by Pseudomonas fluorescens. Geobiology, 8(4), 278–292. https://doi.org/10.1111/j.1472-4669.2010.00241.x
• Fan, D., & Fang, Q. (2021). Siderophores for medical applications: Imaging, sensors, and therapeutics. International Journal of Pharmaceutics, 597, 120306. https://doi.org/10.1016/ j.ijpharm.2021.120306
• Govindarajan, M., Kwon, S. W., & Weon, H. Y. (2007). Isolation, molecular characterization and growth-promoting activities of endophytic sugarcane diazotroph Klebsiella sp. GR9. World Journal of Microbiology and Biotechnology, 23, 997-1006. https://doi.org/10.1007/s11274-006-9326-y
• Guerinot, M. L., Meidl, E. J., & Plessner, O. (1990). Citrate as a siderophore in Bradyrhizobium japonicum. Journal of Bacteriology, 172(6), 3298–3303. https://doi.org/10.1128/jb.172.6.3298-3303.1990
• Haas H. (2003). Molecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage. Applied Microbiology and Biotechnology, 62(4), 316–330. https://doi.org/10.1007/s00253-003-1335-2
• Hofmann, M., Heine, T., Malik, L., Hofmann, S., Joffroy, K., Senges, C. H. R., Bandow, J. E., & Tischler, D. (2021). Screening for Microbial Metal-Chelating Siderophores for the Removal of Metal Ions from Solutions. Microorganisms, 9(1), 111. https://doi.org/10.3390/microorganisms9010111
• Hofmann, M., Heine, T., Schulz, V., Hofmann, S., & Tischler, D. (2019). Draft genomes and initial characteriaztion of siderophore producing pseudomonads isolated from mine dump and mine drainage. Biotechnology Reports (Amsterdam, Netherlands), 25, e00403. https://doi.org/10.1016/j.btre.2019.e00403
• Hussein, K. A., & Joo, J. H. (2014). Potential of siderophore production by bacteria isolated from heavy metal: polluted and rhizosphere soils. Current Microbiology, 68(6), 717–723. https://doi.org/10.1007/s00284-014-0530-y
• Keswani, J., & Whitman, W. B. (2001). Relationship of 16S rRNA sequence similarity to DNA hybridization in prokaryotes. International Journal of Systematic and Evolutionary Microbiology, 51(Pt 2), 667–678. https://doi.org/10.1099/00207713-51-2-667
• Kumar, L., Nagar, S., Mittal, A., Garg, N., & Gupta, V. K. (2014). Immobilization of xylanase purified from Bacillus pumilus VLK-1 and its application in enrichment of orange and grape juices. Journal of Food Science and Technology, 51: 1737-1749. doi: 10.1007/s13197-014-1268-z
• Machuca, A., & Milagres, A. M. (2003). Use of CAS-agar plate modified to study the effect of different variables on the siderophore production by Aspergillus. Letters in Applied Microbiology, 36(3), 177–181. https://doi.org/10.1046/j.1472-765x.2003.01290.x
• Malik, A., & Jaiswal, R. (2000). Metal resistance in Pseudomonas strains isolated from soil treated with industrial wastewater. World Journal of Microbiology and Biotechnology, 16, 177-182. https://doi.org/10.1023/A:1008905902282
• Mehnert, M., Retamal-Morales, G., Schwabe, R., Vater, S., Heine, T., Levicán, G. J., ... & Tischler, D. (2017). Revisiting the chrome azurol S assay for various metal ions. Solid State Phenomena, 262, 509-512. https://doi.org/10.4028/www.scientific.net/SSP.262.509
• Meier-Kolthoff, J. P., Auch, A. F., Klenk, H. P., & Göker, M. (2013). Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics, 14, 60. https://doi.org/10.1186/1471-2105-14-60
• Neilands J. B. (1993). Siderophores. Archives of Biochemistry and Biophysics, 302(1), 1–3. https://doi.org/10.1006/abbi.1993.1172
• Payne S. M. (1994). Detection, isolation, and characterization of siderophores. Methods in Enzymology, 235, 329–344. https://doi.org/10.1016/0076-6879(94)35151-1
• Rajkumar, M., Ae, N., Prasad, M. N., & Freitas, H. (2010). Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends in Biotechnology, 28(3), 142–149. https://doi.org/10.1016/j.tibtech.2009.12.002
• Ribeiro, M., Sousa, C. A., & Simões, M. (2022). Harnessing microbial iron chelators to develop innovative therapeutic agents. Journal of Advanced Research, 39, 89–101. https://doi.org/10.1016/j.jare.2021.10.010
• Rout, M. E., Chrzanowski, T. H., Westlie, T. K., DeLuca, T. H., Callaway, R. M., & Holben, W. E. (2013). Bacterial endophytes enhance competition by invasive plants. American Journal of Botany, 100(9), 1726–1737. https://doi.org/10.3732/ajb.1200577
• Santoyo, G., Moreno-Hagelsieb, G., Orozco-Mosqueda, M.delC., & Glick, B. R. (2016). Plant growth-promoting bacterial endophytes. Microbiological Research, 183, 92–99. https://doi.org/10.1016/j.micres.2015.11.008
• SAS. (2016). SAS® 9.4 Language Reference: Concepts, Sixth Edition. Cary, NC: SAS Institute Inc.
• Schalk, I. J., Hannauer, M., & Braud, A. (2011). New roles for bacterial siderophores in metal transport and tolerance. Environmental Microbiology, 13(11), 2844–2854. https://doi.org/10.1111/j.1462-2920.2011.02556.x
• Schwyn, B., & Neilands, J. B. (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 160(1), 47–56. https://doi.org/10.1016/0003-2697(87)90612-9
• Singh, M., Kumar, A., Singh, R., & Pandey, K. D. (2017). Endophytic bacteria: a new source of bioactive compounds. 3 Biotech, 7(5), 315. https://doi.org/10.1007/s13205-017-0942-z
• Sinha, A. K., Parli Venkateswaran, B., Tripathy, S. C., Sarkar, A., & Prabhakaran, S. (2019). Effects of growth conditions on siderophore producing bacteria and siderophore production from Indian Ocean sector of Southern Ocean. Journal of Basic Microbiology, 59(4), 412–424. https://doi.org/10.1002/jobm.201800537
• Tindall, B. J., Rosselló-Móra, R., Busse, H. J., Ludwig, W., & Kämpfer, P. (2010). Notes on the characterization of prokaryote strains for taxonomic purposes. International Journal of Systematic and Evolutionary Microbiology, 60(Pt 1), 249–266. https://doi.org/10.1099/ijs.0.016949-0
• 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
• Verma, N., & Sharma, R. (2017). Bioremediation of Toxic Heavy Metals: A Patent Review. Recent Patents on Biotechnology, 11(3), 171–187. https://doi.org/10.2174/1872208311666170111111631
• Winkelmann, G. (1979). Surface iron polymers and hydroxy acids. A model of iron supply in sideramine-free fungi. Archives of Microbiology, 121, 43-51. https://doi.org/10.1007/BF00409204