Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Zinc Ions Affect Siderophore Production by Fungi Isolated from the Panax ginseng Rhizosphere

  • Hussein, Khalid Abdallah (Botany and Microbiology Department, Faculty of Science, Assiut University) ;
  • Joo, Jin Ho (Department of Biological Environment, Kangwon National University)
  • Received : 2017.12.11
  • Accepted : 2018.10.09
  • Published : 2019.01.28
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Abstract

Although siderophore compounds are mainly biosynthesized as a response to iron deficiency in the environment, they also bind with other metals. A few studies have been conducted on the impact of heavy metals on the siderophore-mediated iron uptake by microbiome. Here, we investigated siderophore production by a variety of rhizosphere fungi under different concentrations of $Zn^{2+}$ ion. These strains were specifically isolated from the rhizosphere of Panax ginseng (Korean ginseng). The siderophore production of isolated fungi was investigated with chrome azurol S (CAS) assay liquid media amended with different concentrations of $Zn^{2+}$ (50 to $250{\mu}g/ml$). The percentage of siderophore units was quantified using the ultra-violet (UV) irradiation method. The results indicated that high concentrations of $Zn^{2+}$ ion increase the production of siderophore in iron-limited cultures. Maximum siderophore production by the fungal strains was detected at $Zn^{2+}$ ion concentration of $150{\mu}g/ml$ except for Mortierella sp., which had the highest siderophore production at $200{\mu}g/ml$. One potent siderophore-producing strain (Penicillium sp. JJHO) was strongly influenced by the presence of $Zn^{2+}$ ions and showed high identity to P. commune (100% using 18S-rRNA sequencing). The purified siderophores of the Penicillium sp. JJHO strain were chemically identified using UV, Fourier-transform infrared spectroscopy (FTIR), and matrix-assisted laser desorption/ionization time-of-flight mass spectrometer (MALDI-TOF-MS) spectra.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)

References

  1. Pereg L, McMillan M. 2015. Scoping the potential uses of beneficial microorganisms for increasing productivity in cotton cropping systems Soil. Biol. Biochem. 80: 349-358. https://doi.org/10.1016/j.soilbio.2014.10.020
  2. Neubauer U, Nowack B, Furrer G, Schulin R. 2000. Heavy metal sorption on clay minerals affected by the siderophore desferrioxamine B. Environ. Sci. Technol. 34: 2749-2755. https://doi.org/10.1021/es990495w
  3. Aznar A, Dellagi A. 2015. New insights into the role of siderophores as triggers of plant immunity: what can we learn from animals? J. Exper. Bot. 66: 3001-3010. https://doi.org/10.1093/jxb/erv155
  4. Renshaw JC, Robson GD, Trinci APJ, Wiebe MG, Livens FR, Collison D, et al. 2002. Fungal siderophores structures, functions and applications. Mycol. Res. 106: 1123-1142. https://doi.org/10.1017/S0953756202006548
  5. Dimkpa CO, Svatos A, Dabrowska P, Schmidt A, Boland W, Kothe E. 2008. Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74: 19-25. https://doi.org/10.1016/j.chemosphere.2008.09.079
  6. Tripathi M, Munot HP, Shouche Y, Meyer JM, Goel R. 2005. Isolation and functional characterization of siderophore-producing lead- and cadmium-resistant Pseudomonas putida KNP9. Curr. Microbiol. 50: 233-237. https://doi.org/10.1007/s00284-004-4459-4
  7. Bazihizina TC, MartiL RA, Spinelli F, Giordano C, Caparrotta S, Gori M, Azzarello E, Mancuso S. 2014. $Zn^{2+}$ induced changes at the root level account for the increased tolerance of acclimated tobacco plants. J. Exp. Bot. 65: 4931-4942. https://doi.org/10.1093/jxb/eru251
  8. Kabir E, Ray S, Kim K, Yoon H, Jeon E, Kim Y, et al. 2012. Current status of trace metal pollution in soils affected by industrial activities. Scientific World Journal 916705.
  9. Liu M, Lia Y, Zhanga W, Yaojing W. 2013. Assessment and Spatial distribution of zinc pollution in agricultural soils of Chaoyang, China. Procedia Environ. Sci. 18: 283-289. https://doi.org/10.1016/j.proenv.2013.04.037
  10. Johnstone TC, Nolan EM. 2015. Beyond iron: non-classical biological functions of bacterial siderophores. Dalton Trans. 14: 6320-6339. https://doi.org/10.1039/C4DT03559C
  11. Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P. 2016. Microbial siderophores and their potential applications: a review. Environ. Sci. Pollut. Res. Int. 23: 3984-3999. https://doi.org/10.1007/s11356-015-4294-0
  12. Ahmed E, Holmstrom SJM. 2014. Siderophores in environmental research: roles and applications: minireview. Microb. Biotechnol. 7: 196-208. https://doi.org/10.1111/1751-7915.12117
  13. Schwyn B, Neilands, J.B. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56. https://doi.org/10.1016/0003-2697(87)90612-9
  14. Naidu AJ, Yadav M. 1997. Influence of iron, growth temperature and plasmids on siderophore production in Aerornonas hydrophila. J. Med. Microbiol. 47: 833-838. https://doi.org/10.1099/00222615-46-10-833
  15. Hussein KA, Joo JH. 2017. Stimulation, purification, and chemical characterization of siderophores produced by the rhizospheric bacterial strain Pseudomonas putida. Rhizosphere 4: 16-21. https://doi.org/10.1016/j.rhisph.2017.05.006
  16. Qi Z. 1997. Fungi of China: Aspergillus et teleomorphi cognate. pp. 76-82. (Vol.5) Science Press, Beijing, China,.
  17. Kong H. 2007. Flora Fungorum Sinicorum. pp. 283. (Vol. 35): Penicillium et teleomorphi cognati. Science Press, Beijing.
  18. Zhang Z. 2003. Cladosporium, Fusicladium, Pyricularia. Flora Fungorum Sinicorum. pp. 297. (Vol. 14) Science Press, Beijing, China.
  19. Herlemann DP, Labrenz M, Jurgens K, Bertilsson S, Waniek JJ, Andersson AF. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 5: 1571-1579. https://doi.org/10.1038/ismej.2011.41
  20. Thompson J, Higgins D, Gibson T. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment thr ough sequence weighting, positionspecific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680. https://doi.org/10.1093/nar/22.22.4673
  21. Csaky TZ. 1948. On the estimation of bound hydroxylamines in biological materials. Acta Chem. Scand. 2: 450-454. https://doi.org/10.3891/acta.chem.scand.02-0450
  22. Arnow LE. 1937. Colorimetric determination of the components of 3,4-dihydroxyphenylalanine tyrosine mixtures. J. Biol. Chem. 118: 531-537. https://doi.org/10.1016/S0021-9258(18)74509-2
  23. SAS Institute Inc, SAS, SAS/STAT 9.1 User's Guide. 2004. SAS Institute Inc., Cary, NC, USA.
  24. Ahmed E, Holmstrom SJM. 2014. Siderophores in environmental research: roles and applications Microb. Biotechnol. 7: 196-208. https://doi.org/10.1111/1751-7915.12117
  25. Hussein KA, Joo JH. 2012. Comparison between Siderophores Production by Fungi Isolated from Heavy Metals Polluted and Rhizosphere Soils. Kor. J. Soil Sci. Fert. 45: 798-804. https://doi.org/10.7745/KJSSF.2012.45.5.798
  26. Rajkumar M, Freitas H. 2009. Effects of inoculation of plantgrowth promoting bacteria on Ni uptake by Indian mustard. Bioresour. Technol. 99: 3491-3498. https://doi.org/10.1016/j.biortech.2007.07.046
  27. Yamasaki S, Sakata-Sogawa K, Hasegawa A. 2007. Zinc is a novel intracellular second messenger. J. Cell Biol. 177: 637-645. https://doi.org/10.1083/jcb.200702081
  28. Huang J, Canadien V, Lam GY. 2009. Activation of antibacterial autophagy by NADPH oxidases. Proc. Natl. Acad. Sci. USA 106: 6226-6231. https://doi.org/10.1073/pnas.0811045106
  29. Corbin BD, Seeley EH, Raab A. Feldmann J, Miller MR, Torres VJ, Anderson KL, et al. 2008. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 15: 962-965.
  30. Schwecke T, Goettling, K, Durek P, Duenas I, Kaeufer NF, Zock ES, et al. 2006. Nonribosomal peptide synthesis in Schizosaccharomyces pombe and the architectures of ferrichrome-type siderophore synthetases in fungi. Chem. Biochem. 7: 612-622.
  31. Rossbach S, Wilson TL, Kukuk ML, Carty HA. 2000. Elevated zinc induces siderophore biosynthesis genes and a zntA-like gene in Pseudomonas fluorescens. FEMS Microbiol. Lett. 1: 61-70.
  32. Carroll CS, Nesbitt JR, Henry KA, Pinto LJ, Moinzadeh M, Scott JK, et al. 2012. Structural requirements for the activity of the MirB ferrisiderophore transporter of Aspergillus fumigates isabelle raymond-bouchard. Eukaryot Cell. 11: 1333-1344. https://doi.org/10.1128/EC.00159-12
  33. Eisendle M, Oberegger H, Zadra I, Haas H. 2003. The siderophore system is essential for viability of Aspergillus nidulans: functionalanalysis of two genes encoding lornithine N 5-monooxygenase (sidA) and a non-ribosomal peptide synthetase (sidC). Mol. Microbiol. 49: 359-375. https://doi.org/10.1046/j.1365-2958.2003.03586.x
  34. Plattner H, Diekmann H. 1994. Enzymology of siderophore biosynthesis. In Metal Ions in Fungi (G. Winkelmann & D. R. Winge, eds) pp. 99-116. Marcel Dekker, New York.
  35. Grundlinger M, Yasmin S, Lechner BE, Geley S, Schrett M, Hynes M, et al. 2013. Fungal siderophore biosynthesis is partially localized in peroxisomes. Mol. Microbiol. 88: 862-875. https://doi.org/10.1111/mmi.12225
  36. Frisvad JC, Larsen TO. 2016 Extrolites of Aspergillus fumigatus and other pathogenic species in Aspergillus section fumigati. Front. Microbiol. 6: 1485. https://doi.org/10.3389/fmicb.2015.01485
  37. Miethke M, Marahiel MA. 2007. Siderophore-based iron acquisition and pathogen control. Mol. Biol. Rev. 71: 3413-4511.
  38. Weaver RS, Kirchman DL, David A. 2003. Hutchins Utilization of iron/organic ligand complexes by marine bacterioplankton aquatic microbial ecology. Aquat. Microb. Ecol. 31: 227-239. https://doi.org/10.3354/ame031227
  39. Masuda T, Hayashi J, Tamagaki S. 2000. $C_3$-symmetric ferrichrome-mimicking $Fe^{3+}$ complexes containing the 1-hydroxypyrimidinone $Fe^{3+}$ binding moieties based on ${\alpha}$-cyclodextrin: helicities in solvent environments. J. Chem. Soci. Perkin Trans. 2: 161-167. https://doi.org/10.1039/a904153b
  40. Hannauer M, Barda Y, Mislin GA, Shanzer A, Schalk IJ. 2010. The ferrichrome uptake pathway in Pseudomonas aeruginosa involves an iron release mechanism with acylation of the siderophore and recycling of the modified desferrichrome. J. Bacteriol. 192: 1212-1220. https://doi.org/10.1128/JB.01539-09
  41. Tedstone AA, Lewis DJ, Brien P. 2016. Synthesis, properties, and applications of transition metal-doped layered transition metal dichalcogenides. Chem. Mater. 28: 1965-1974. https://doi.org/10.1021/acs.chemmater.6b00430
  42. Dimkpa C. 2016. Microbial siderophores: production, detection and application in agriculture and environment. Endocytobiosis Cell Res. 27: 7-16.
  43. Krober A, Scherlach K, Hortschansky P, Shelest E, Staib P, Kniemeyer O, et al. 2016. HapX mediates iron homeostasis in the pathogenic dermatophyte Arthroderma benhamiae but is dispensable for virulence. PLoS One 11: e0150701. https://doi.org/10.1371/journal.pone.0150701
  44. Bushley KE, Ripolland DR, Turgeon B. 2008. Module evolution and substrate specificity of fungal nonribosomal peptide synthetases involved in siderophore biosynthesis. BMC Evoly. Biol. 8: 328. https://doi.org/10.1186/1471-2148-8-328
  45. Bushley KE, Turgeon BG, 2010. Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol. Biol. 10: 26. https://doi.org/10.1186/1471-2148-10-26

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