Journal of Microbiology and Biotechnology
The Korean Society for Microbiology and Biotechnology publishes the Journal of Microbiology and Biotechnology.

2019 ; Vol.29-1: 105~113

AuthorKhalid Abdallah Hussein, Jin Ho Joo
Place of dutyBotany and Microbiology Department, Faculty of Science, Assiut University, 71516, Assiut, Egypt,Department of Biological Environment, Kangwon National University, Chuncheon, Kangwon-do, Republic of Korea
TitleZinc Ions Affect Siderophore Production by Fungi Isolated from the Panax ginseng Rhizosphere
PublicationInfo J. Microbiol. Biotechnol.2019 ; Vol.29-1
AbstractAlthough 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 Zn2+ 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 Zn2+ (50 to 250 μg/ml). The percentage of siderophore units was quantified using the ultra-violet (UV) irradiation method. The results indicated that high concentrations of Zn2+ ion increase the production of siderophore in iron-limited cultures. Maximum siderophore production by the fungal strains was detected at Zn2+ ion concentration of 150 μg/ml except for Mortierella sp., which had the highest siderophore production at 200 μg/ml. One potent siderophoreproducing strain (Penicillium sp. JJHO) was strongly influenced by the presence of Zn2+ 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, Fouriertransform infrared spectroscopy (FTIR), and matrix-assisted laser desorption/ionization timeof- flight mass spectrometer (MALDI-TOF-MS) spectra.
Full-Text
Key_wordRoot-associated fungi, siderophores, Zn2+, Penicillium commune
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.
    CrossRef
  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.
    CrossRef
  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.
    Pubmed CrossRef
  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.
    CrossRef
  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.
    Pubmed CrossRef
  6. Tripathi M, Munot HP, Shouche Y, Meyer JM, Goel R. 2005. Isolation and functional characterization of siderophoreproducing lead- and cadmium-resistant Pseudomonas putida KNP9. Curr. Microbiol. 50: 233-237.
    Pubmed CrossRef
  7. Bazihizina TC, MartiL RA, Spinelli F, Giordano C, Caparrotta S, Gori M, Azzarello E, Mancuso S. 2014. Zn2+ induced changes at the root level account for the increased tolerance of acclimated tobacco plants. J. Exp. Bot. 65: 4931-4942.
    Pubmed CrossRef Pubmed Central
  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. Sci. World J. Article ID 916705.
    Pubmed CrossRef Pubmed Central
  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.
    CrossRef
  10. Johnstone TC, Nolan EM. 2015. Beyond iron: non-classical biological functions of bacterial siderophores. Dalton Trans. 14: 6320-6339.
    Pubmed CrossRef Pubmed Central
  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.
    Pubmed CrossRef
  12. Ahmed E, Holmstrom SJM. 2014. Siderophores in environmental research: roles and applications: minireview. Microb. Biotechnol. 7: 196-208.
    Pubmed CrossRef Pubmed Central
  13. Schwyn B, Neilands, J.B. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56.
    CrossRef
  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.
    Pubmed CrossRef
  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.
    CrossRef
  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, Jürgens 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.
    Pubmed CrossRef Pubmed Central
  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.
    Pubmed CrossRef Pubmed Central
  21. Csáky TZ. 1948. On the estimation of bound hydroxylamines in biological materials. Acta Chem. Scand. 2: 450-454.
    CrossRef
  22. Arnow LE. 1937. Colorimetric determination of the components of 3,4-dihydroxyphenylalanine tyrosine mixtures. J. Biol. Chem. 118: 531-537.
  23. SAS Institute Inc, SAS, SAS/STAT 9.1 User’s Guide. 2004. SAS Institute Inc., Cary, NC, USA.
  24. Ahmed E, Holmström SJM. 2014. Siderophores in environmental research: roles and applications Microb. Biotechnol. 7: 196-208.
    Pubmed CrossRef Pubmed Central
  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.
    CrossRef
  26. Rajkumar M, Freitas H. 2009. Effects of inoculation of plantgrowth promoting bacteria on Ni uptake by Indian mustard. Bioresour. Technol. 99: 3491-3498.
    Pubmed CrossRef
  27. Yamasaki S, Sakata-Sogawa K, Hasegawa A. 2007. Zinc is a novel intracellular second messenger. J. Cell Biol. 177: 637-645.
    Pubmed CrossRef Pubmed Central
  28. Huang J, Canadien V, Lam GY. 2009. Activation of antibacterial autophagy by NADPH oxidases. Proc. Natl. Acad. Sci. USA 106: 6226-6231.
    Pubmed CrossRef Pubmed Central
  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.
    Pubmed CrossRef
  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 ferrichrometype siderophore synthetases in fungi. Chem. Biochem. 7:612-622.
    Pubmed CrossRef
  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.
    Pubmed CrossRef
  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.
    Pubmed CrossRef Pubmed Central
  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.
    Pubmed CrossRef
  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. Gründlinger 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.
    Pubmed CrossRef Pubmed Central
  36. Frisvad JC, Larsen TO. 2016 Extrolites of Aspergillus fumigatus and other pathogenic species in Aspergillus section fumigati. Front. Microbiol. 6: 1485.
    Pubmed CrossRef Pubmed Central
  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.
    CrossRef
  39. Masuda T, Hayashi J, Tamagaki S. 2000. C3-symmetric ferrichrome-mimicking Fe3+complexes containing the 1hydroxypyrimidinone Fe3+ binding moieties based on αcyclodextrin: helicities in solvent environments. J. Chem. Soci. Perkin Trans. 2: 161-167.
    CrossRef
  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.
    Pubmed CrossRef Pubmed Central
  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.
    CrossRef
  42. Dimkpa C. 2016. Microbial siderophores: production, detection and application in agriculture and environment. Endocytobiosis Cell Res. 27: 7-16.
  43. Kröber 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.
    Pubmed CrossRef Pubmed Central
  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.
    Pubmed CrossRef Pubmed Central
  45. Bushley KE, Turgeon BG, 2010. Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol. Biol. 10: 26.
    Pubmed CrossRef Pubmed Central



Copyright © 2009 by the Korean Society for Microbiology and Biotechnology.
All right reserved. Mail to jmb@jmb.or.kr
Online ISSN: 1738-8872    Print ISSN: 1017-7825    Powered by INFOrang.co., Ltd