Environmental Science and Pollution Research

, Volume 23, Issue 5, pp 3984–3999 | Cite as

Microbial siderophores and their potential applications: a review

  • Maumita Saha
  • Subhasis Sarkar
  • Biplab Sarkar
  • Bipin Kumar Sharma
  • Surajit Bhattacharjee
  • Prosun Tribedi
Review Article


Siderophores are small organic molecules produced by microorganisms under iron-limiting conditions which enhance the uptake of iron to the microorganisms. In environment, the ferric form of iron is insoluble and inaccessible at physiological pH (7.35–7.40). Under this condition, microorganisms synthesize siderophores which have high affinity for ferric iron. These ferric iron-siderophore complexes are then transported to cytosol. In cytosol, the ferric iron gets reduced into ferrous iron and becomes accessible to microorganism. In recent times, siderophores have drawn much attention due to its potential roles in different fields. Siderophores have application in microbial ecology to enhance the growth of several unculturable microorganisms and can alter the microbial communities. In the field of agriculture, different types of siderophores promote the growth of several plant species and increase their yield by enhancing the Fe uptake to plants. Siderophores acts as a potential biocontrol agent against harmful phyto-pathogens and holds the ability to substitute hazardous pesticides. Heavy-metal-contaminated samples can be detoxified by applying siderophores, which explicate its role in bioremediation. Siderophores can detect the iron content in different environments, exhibiting its role as a biosensor. In the medical field, siderophore uses the “Trojan horse strategy” to form complexes with antibiotics and helps in the selective delivery of antibiotics to the antibiotic-resistant bacteria. Certain iron overload diseases for example sickle cell anemia can be treated with the help of siderophores. Other medical applications of siderophores include antimalarial activity, removal of transuranic elements from the body, and anticancer activity. The aim of this review is to discuss the important roles and applications of siderophores in different sectors including ecology, agriculture, bioremediation, biosensor, and medicine.


Iron Siderophore Microbial ecology Bioremediation Biosensor Medicine 



The authors would like to thank Manash Chandra Das, Priya Gupta, and Antu Das for their valuable contributions for the improvement of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Ackrill P, Raiston AJ, Day JP, Hoodge KC (1980) Successful removal of aluminum from patients with encephalopathy. Lancet 2:692–693CrossRefGoogle Scholar
  2. Ahmed E, Holmstrom SJM (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7:196–208CrossRefGoogle Scholar
  3. Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by Rhizosphere bacteria. Biol Fertil Soils 12:39–45CrossRefGoogle Scholar
  4. Ali SS, Vidhale NN (2013) Bacterial siderophore and their application: a review. Int J Curr Microbiol Appl Sci 2:303–312Google Scholar
  5. Arze RS, Parkinson IS, Cartilidge NEF, Britton P, Ward MK (1981) Reversal of aluminium dialysis encephalopathy after desferrioxamine treatment. Lancet 318(8255):1116CrossRefGoogle Scholar
  6. Barbeau K, Rue EL, Trick CG, Bruland KW, Butler A (2003) Photochemical reactivity of siderophores produced by marine heterotrophic bacteria and Cyanobacteria based on characteristic Fe (III) binding groups. Limnol Oceanogr 48(3):1069–1078CrossRefGoogle Scholar
  7. Barrero JM, Moreno-Bondi MC, Perez-Conde MC, Camara C (1993) A biosensor for ferric ion. Talanta 40(11):1619–1623CrossRefGoogle Scholar
  8. Beasley FC, Marolda CL, Cheung J, Buac S, Heinrichs DE (2011) Staphylococcus aureus transporters Hts, Sir, and Sst capture iron liberated from human transferrin by Staphyloferrin A, Staphyloferrin B, and catecholamine stress hormones, respectively, and contribute to virulence. Infect Immun 79:2345–2355CrossRefGoogle Scholar
  9. Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting Rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051CrossRefGoogle Scholar
  10. Bingham FT, Pereyea FJ, Jarrell WM (1986) Metal toxicity to agricultural crops. Met Ions Biol Syst 20:119–156Google Scholar
  11. Blatt J, Stitely S (1987) Antineuroblastoma activity of desferoxamine in human cell lines. Cancer Res 47:1749–1750Google Scholar
  12. Blatt J, Taylor SR, Stitely S (1988) Mechanism of antineuroblastoma activity of deferoxamine in vitro. J Lab Clin Med 112:433–436Google Scholar
  13. Bollard EG (1983) Involvement of unusual elements in plant growth and nutrition. Encyclopedia of plant physiology. New seriesGoogle Scholar
  14. Bou-Abdallah F (2010) The iron redox and hydrolysis chemistry of the ferritins. Biochim Biophys Acta Gen Subj 1800(8):719–731CrossRefGoogle Scholar
  15. Boukhalfa H, Lack JG, Reilly SD, Hersman L, Neu MP (2003) Siderophore production and facilitated uptake of iron and plutonium in P. putida. No. LA-UR-03-0913. Los Alamos National LaboratoryGoogle Scholar
  16. Braud A, Hoegy F, Jezequel K, Lebeau T, Schalk IJ (2009a) New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ Microbiol 11:1079–1091CrossRefGoogle Scholar
  17. Braud A, Jezequel K, Bazot S, Lebeau T (2009b) Enhanced phytoextraction of an agricultural Cr-and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286CrossRefGoogle Scholar
  18. Braun V, Pramanik A, Gwinner T, Koberle M, Bohn E (2009) Sideromycins: tools and antibiotics. BioMetals 22:3–13CrossRefGoogle Scholar
  19. Briat JF, Fobis‐Loisy I, Grignon N, Lobreaux S, Pascal N, Savino G, Thoiron S, Wiren N, Wuytswinkel O (1995) Cellular and molecular aspects of iron metabolism in plants. Biol Cell 84:69–81CrossRefGoogle Scholar
  20. Brinton LA, Gridley G, Persson I, Baron J, Bergqvist A (1997) Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol 176:572–579CrossRefGoogle Scholar
  21. Brochu AN, Brochu TI, Nicas TR, Parr AA, Minnick EK, Dolence JA, McKee MJ, Miller MC, Lavoie MF (1992) Modes of action and inhibitory activities of new siderophore-beta-lactam conjugates that use specific iron uptake pathways for entry into bacteria. Antimicrob Agents Chemother 36:2166–2175CrossRefGoogle Scholar
  22. Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245CrossRefGoogle Scholar
  23. Burt WR, Underwood AL, Appleton GL (1981) Hydroxamic acid from Histoplasma capsulatum that displays growth factor activity. Appl Environ Microbiol 42:560–563Google Scholar
  24. Buss JL, Torti FM, Torti SV (2003) The role of iron chelation in cancer therapy. Curr Med Chem 10:1021–1034CrossRefGoogle Scholar
  25. 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. Microbiol Res 164:570–577CrossRefGoogle Scholar
  26. Cai Y, Wang R, An MM, Bei-Bei L (2010) Iron-depletion prevents biofilm formation in Pseudomonas aeruginosa through twitching motility and quorum sensing. Braz J Microbiol 41(1):37–41CrossRefGoogle Scholar
  27. Campbell JA (1940) Effects of precipitated silica and of iron oxide on the incidence of primary lung tumours in mice. Br Med J 2(4156):275CrossRefGoogle Scholar
  28. Carson JK, Rooney D, Gleeson DB, Clipson N (2007) Altering the mineral composition of soil causes a shift in microbial community structure. FEMS Microbiol Ecol 61:414–423CrossRefGoogle Scholar
  29. Carson JK, Campbell L, Rooney D, Clipson N, Gleeson DB (2009) Minerals in soil select distinct bacterial communities in their microhabitats. FEMS Microbiol Ecol 67:381–388CrossRefGoogle Scholar
  30. Chincholkar SB, Chaudhari BL, Rane MR (2007) Microbial siderophore: a state of art. In A. Varma & S.B. Chincholkar (Eds.), Soil Biology (Vol. 12, pp. 233–242). Berlin, Heidelberg: SpringerGoogle Scholar
  31. Chua AC, Ingram HA, Raymond KN, Baker E (2003) Multidentate pyridinones inhibit the metabolism of nontransferrin‐bound iron by hepatocytes and hepatoma cells. Eur J Biochem 270:1689–1698CrossRefGoogle Scholar
  32. Chung Chun Lam CK, Jickells TD, Richardson DJ, Russell DA (2006) Fluorescence-based siderophore biosensor for the determination of bioavailable iron in oceanic waters. Anal Chem 78:5040–5045CrossRefGoogle Scholar
  33. Ciche TA, Blackburn M, Carney JR, Ensign JC (2003) Photobactin: a catechol siderophore produced by Photorhabdus luminescens, an entomopathogen mutually associated with Heterorhabditis bacteriophora NC1 nematodes. Appl Environ Microbiol 69:4706–4713CrossRefGoogle Scholar
  34. Crowley DA (2006) Microbial siderophores in the plant rhizosphere. In: Barton LL, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands, pp 169–189CrossRefGoogle Scholar
  35. D’Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E, Epstein S, Clardy J, Lewis K (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17:254–264CrossRefGoogle Scholar
  36. Dave BP, Dube HC (2000) Chemical characterization of fungal siderophores. Indian J Exp Biol 38:56–62Google Scholar
  37. Dave BP, Anshuman K, Hajela P (2006) Siderophores of halophilic archaea and their chemical characterization. Indian J Exp Biol 44:340–344Google Scholar
  38. Dertz EA, Xu J, Stintzi A, Raymond KN (2006) Bacillibactin-mediated iron transport in Bacillus subtilis. J Am Chem Soc 128:22–23CrossRefGoogle Scholar
  39. Diekmann H, Zahner H (1967) Konstitution von Fusigen und dessen Abbau zu Δ2‐Anhydromevalonsaurelacton. Eur J Biochem 3(2):213–218CrossRefGoogle Scholar
  40. Drechsel H, Tschierske M, Thieken A, Jung G, Zahner H, Winkelmann G (1995) The carboxylate type siderophore rhizoferrin and its analogs produced by directed fermentation. J Ind Microbiol 14:105–112CrossRefGoogle Scholar
  41. Edberg F, Kalinowski BE, Holmstrom SJ, Holm K (2010) Mobilization of metals from uranium mine waste: the role of pyoverdines produced by Pseudomonas fluorescens. Geobiology 8:278–292CrossRefGoogle Scholar
  42. Eggins BR (1996) Biosensors: an introduction. Wiley, Chichester, UK, pp 16–19Google Scholar
  43. Eldridge ML, Cadotte MW, Rozmus AE, Wilhelm SW (2007) The response of bacterial groups to changes in available iron in the Eastern subtropical Pacific Ocean. J Exp Mar Biol Ecol 348(1):11–22CrossRefGoogle Scholar
  44. Elford HL, Freese M, Passamani E, Morris HP (1970) Ribonucleotide reductase and cell proliferation I. Variations of ribonucleotide reductase activity with tumor growth rate in a series of rat hepatomas. J Biol Chem 245(20):5228–5233Google Scholar
  45. Essen SA, Johnsson A, Bylund D, Pedersen K, Lundstrom US (2007) Siderophore production by Pseudomonas stutzeri under aerobic and anaerobic conditions. Appl Environ Microbiol 73(18):5857–5864CrossRefGoogle Scholar
  46. Fardeau S, Mullie C, Dassonville-Klimpt A, Audic N, Sonnet P (2011) Bacterial iron uptake: a promising solution against multidrug resistant bacteria. In Science against microbial pathogens: communicating current research and technological advances, pp. 695–705Google Scholar
  47. Fiedler HP, Krastel P, Müller J, Gebhardt K, Zeeck A (2001) Enterobactin: the characteristic catecholate siderophore of Enterobacteriaceae is produced by Streptomyces species. FEMS Microbiol Lett 196:147–151CrossRefGoogle Scholar
  48. Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress and antioxidant nutrients. Toxicology 189:147–163CrossRefGoogle Scholar
  49. Gamalero E, Glick BR (2011) Mechanisms used by plant growth-promoting bacteria. In Bacteria in Agrobiology: Plant Nutrient Management. Springer Berlin Heidelberg, 17–46Google Scholar
  50. Gamit DA, Tank SK (2014) Effect of siderophore producing microorganism on plant growth of Cajanus cajan (Pigeon pea). Int J Res Pure Appl Microbiol 4:20–27Google Scholar
  51. Gangwar M, Kaur G (2009) Isolation and characterization of endophytic bacteria from endorhizosphere of sugarcane and ryegrass. Internet J Microbiol 7:139–144Google Scholar
  52. Gledhill M (2001) Electrospray ionisation-mass spectrometry of hydroxamate siderophores. Analyst 126(8):1359–1362CrossRefGoogle Scholar
  53. Glick R, Gilmour C, Tremblay J, Satanower S, Avidan O, Deziel E, Greenberg EP, Poole K, Banin E (2010) Increase in rhamnolipid synthesis under iron-limiting conditions influences surface motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 192(12):2973–2980CrossRefGoogle Scholar
  54. Gorska A, Sloderbach A, Marszall MP (2014) Siderophore-drug complexes: potential medicinal applications of the ‘Trojan horse’ strategy. Trends Pharmacol Sci 35(9):442–449CrossRefGoogle Scholar
  55. Griffiths GL, Sigel SP, Payne SM, Neilands JB (1984) Vibriobactin, a siderophore from Vibrio cholerae. J Biol Chem 259(1):383–385Google Scholar
  56. Guan LL, Kamino K (2001) Bacterial response to siderophore and quorum-sensing chemical signals in the seawater microbial community. BMC Microbiol 1(1):27CrossRefGoogle Scholar
  57. Gupta V, Saharan K, Kumar L, Gupta R, Sahai V, Mittal A (2008) Spectrophotometric ferric ion biosensor from Pseudomonas fluorescens culture. Biotechnol Bioeng 100(2):284–296CrossRefGoogle Scholar
  58. Gutteridge JM, Rowley DA, Halliwell B (1982) Superoxide-dependent formation of hydroxyl radicals and lipid peroxidation in the presence of iron salts: detection of ‘catalytic’ iron and anti-oxidant activity in extracellular fluids. Biochem J 206:605–609CrossRefGoogle Scholar
  59. Gysin J, Crenn Y, Pereira Da Silva L, Breton C (1991) Siderophores as anti parasitic agents. US Patent (US 5192807 A) 5:192–807Google Scholar
  60. Hamdan H, Weller DM, Thomashow LS (1991) Relative importance of fluorescent siderophores and other factors in biological control of Gaeumannomyces graminis var. Tritici by Pseudomonas fluorescens 2–79 and M4-80R. Appl Environ Microbiol 57:3270–3277Google Scholar
  61. Hansen TV, Aaxeth J, Alexander J (1982) The effect of chelating agents on vanadium distribution in the rat body and on uptake by human erythrocytes. Arch Toxicol 50:195–202CrossRefGoogle Scholar
  62. Hantke K, Nicholson G, Rabsch W, Winkelmann G (2003) Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci 100:3677–3682CrossRefGoogle Scholar
  63. He ZL, Yang XE (2007) Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J Zhejiang Univ Sci B 8(3):192–207CrossRefGoogle Scholar
  64. Heldal M, Norland S, Tumyr O (1985) X-ray microanalytic method for measurement of dry matter and elemental content of individual bacteria. Appl Environ Microbiol 50:1251–1257Google Scholar
  65. Hershko C, Link G, Konijn AM (2002) Cardioprotective effect of iron chelators, in iron chelation theraphy. Vol 509. Springer, New York US. 1 Ed, pp 77–89Google Scholar
  66. Hofte M (1993) Classes of microbial siderophores. Iron chelation in plants and soil microorganisms. Academic Press Inc 3–26Google Scholar
  67. Holinsworth B, Martin JD (2009) Siderophore production by marine-derived fungi. BioMetals 22(4):625–632CrossRefGoogle Scholar
  68. Holzberg M, Artis WM (1983) Hydroxamate siderophore production by opportunistic and systemic fungal pathogens. Infect Immun 40:1134–1139Google Scholar
  69. Huang Y, Jiang Y, Wang H, Wang J, Shin MC, Byun Y, He H, Liang Y, Yang VC (2013) Curb challenges of the “Trojan Horse” approach: smart strategies in achieving effective yet safe cell-penetrating peptide-based drug delivery. Adv Drug Deliv Rev 65(10):1299–1315CrossRefGoogle Scholar
  70. Huber DL (2005) Synthesis, properties, and applications of iron nanoparticles. Small 1(5):482–501CrossRefGoogle Scholar
  71. Ines M, Amel K, Yousra T, Neila S, Imen D, Marie MJ, Abdennasseur H (2012) Effect of dose–response of zinc and manganese on siderophores production. Am J Environ Sci 8(2):143–151CrossRefGoogle Scholar
  72. Jin CW, Li GX, Yu XH, Zheng SJ (2010) Plant Fe status affects the composition of siderophore-secreting microbes in the rhizosphere. Annals of botany, mcq 071Google Scholar
  73. Jin CW, Ye YQ, Zheng SJ (2014) An underground tale: contribution of microbial activity to plant iron acquisition via ecological processes. Ann Bot 113(1):7–18CrossRefGoogle Scholar
  74. Joshi FR, Desai DK, Archana G, Desai AJ (2009) Enhanced survival and nodule occupancy of pigeon pea nodulating Rhizobium sp. ST1 expressing feg A gene of Bradyrhizobium japonicum 61A152. On Line J Biol Sci 9:40–51CrossRefGoogle Scholar
  75. Kaeberlein T, Lewis K, Epstein SS (2002) Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:1127–1129CrossRefGoogle Scholar
  76. Kannahi M, Senbagam N (2014) Studies on siderophore production by microbial isolates obtained from rhizosphere soil and its antibacterial activity. J Chem Pharm Res 6:1142–1145Google Scholar
  77. Keller M, Zengler K (2004) Tapping into microbial diversity. Nat Rev Microbiol 2:141–150CrossRefGoogle Scholar
  78. Kim JJ, Masui R, Kuramitsu S, Seo JH, Kim K, Sung MH (2008) Characterization of growth-supporting factors produced by Geobacillus toebii for the commensal thermophile Symbiobacterium toebii. J Microbiol Biotechnol 18(3):490–496Google Scholar
  79. Kim K, Kim JJ, Masui R, Kuramitsu S, Sung MH (2011) A commensal symbiotic interrelationship for the growth of Symbiobacterium toebii with its partner bacterium, Geobacillus toebii. BMC Res Note 4:437CrossRefGoogle Scholar
  80. Kloepper JW, Leong J, Teintze M, Schiroth MN (1980) Enhanced plant growth by siderophores produced by plant growth promoting Rhizobacteria. Nature 286:885–886CrossRefGoogle Scholar
  81. Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci 66:3–18CrossRefGoogle Scholar
  82. Krewulak KD, Vogel HJ (2008) Structural biology of bacterial iron uptake. Biochim Biophys Acta Biomembr 1778(9):1781–1804CrossRefGoogle Scholar
  83. Lacava PT, Silva-Stenico ME, Araujo WL, Simionato AVC, Carrilho E, Tsai SM, Azevedo JL (2008) Detection of siderophores in endophytic bacteria Methylobacterium spp. associated with Xylella fastidiosa subsp. pauca. Pesq Agrop Brasileira 43(4):521–528CrossRefGoogle Scholar
  84. Lehner SM, Atanasova L, Neumann NK, Krska R, Lemmens M, Druzhinina IS, Schuhmacher R (2013) Isotope-assisted screening for iron-containing metabolites reveals a high degree of diversity among known and unknown siderophores produced by Trichoderma spp. Appl Environ Microbiol 79(1):18–31CrossRefGoogle Scholar
  85. Leong SA, Neilands JB (1982) Siderophore production by phytopathogenic microbial species. Arch Biochem Biophys 281:351–359CrossRefGoogle Scholar
  86. Lewis K, Epstein S, D’Onofrio A, Ling LL (2010) Uncultured microorganisms as a source of secondary metabolites. J Antibiot 63(8):468–476CrossRefGoogle Scholar
  87. Lovejoy DB, Richardson DR (2003) Iron chelators as anti-neoplastic agents: current developments and promise of the PIH class of chelators. Cur Med Chem 10:1035–1049CrossRefGoogle Scholar
  88. Loyevsky M, Lytton SD, Mester B, Libman J, Shanzer A, Cabantchik ZI (1993) The antimalareial action of desferal involves a direct access route to erythrocytic (Plasmodium falciparum) parasites. J Clin Investig 91:218–224CrossRefGoogle Scholar
  89. Loyevsky M, John C, Dickens B, Hu V, Miller JH, Gordeuk VR (1999) Chelation of iron within the erythrocytic Plasmodium falciparum parasite by iron chelators. Mol Biochem Parasitol 101:43–59CrossRefGoogle Scholar
  90. Marschner H, Romheld V, Kissel M (1986) Different strategies in higher plants in mobilization and uptake of iron. J Plant Nutr 9:695–713CrossRefGoogle Scholar
  91. Masalha J, Kosegarten H, Elmaci O, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soils 30:433–439CrossRefGoogle Scholar
  92. Matsumoto K, Ozawa T, Jitsukawa K, Masuda H (2004) Synthesis, solution behavior, thermal stability, and biological activity of an Fe (III) complex of an artificial siderophore with intramolecular hydrogen bonding networks. Inorg Chem 43:8538–8546CrossRefGoogle Scholar
  93. Maurer B, Keller-Schierlein W (1968) Ferribactin, a Siderochrome from Pseudomonas fluorescens Migula: 61. Mitteilung Ferribactin, ein Siderochromaus Pseudomonas fluorescens Migula. Arch Microbiol 60:326–339Google Scholar
  94. May JJ, Wendrich TM, Marahiel MA (2001) The dhb Operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2, 3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276:7209–7217CrossRefGoogle Scholar
  95. McCormack P, Worsfold PJ, Gledhill M (2003) Separation and detection of siderophores produced by marine bacterioplankton using high-performance liquid chromatography with electrospray ionization mass spectrometry. Anal Chem 75(11):2647–2652CrossRefGoogle Scholar
  96. McLoughlin TJ, Quinn JP, Bettermann A, Bookland R (1992) Pseudomonas cepacia suppression of sunflower wilt fungus and role of antifungal compounds in controlling the disease. Appl Environ Microbiol 58(5):1760–1763Google Scholar
  97. Meiwes J, Fiedler HP, Haag H, Zahner H, Konetschny-Rapp S, Jung G (1990) Isolation and characterization of Staphyloferrin A, a compound with siderophore activity from Staphylococcus hyicus DSM 20459. FEMS Microbiol Lett 67:201–206CrossRefGoogle Scholar
  98. Messenger AJ, Barclay R (1983) Bacteria, iron and pathogenicity. Biochem Educ 11(2):54–63CrossRefGoogle Scholar
  99. Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451CrossRefGoogle Scholar
  100. Milner SJ, Seve A, Snelling AM, Thomas GH, Kerr KG, Routledge A, Duhme-Klair AK (2013) Staphyloferrin A as siderophore-component in fluoroquinolone-based Trojan horse antibiotics. Org Biomol Chem 11(21):3461–3468CrossRefGoogle Scholar
  101. Mollmann U, Heinisch L, Bauernfeind A, Kohler T, Ankel-Fuchs D (2009) Siderophores as drug delivery agents: application of the “Trojan Horse” strategy. Biometals 22(4):615–624CrossRefGoogle Scholar
  102. Murugappan RM, Aravinth A, Karthikeyan M (2011) Chemical and structural characterization of hydroxamate siderophore produced by marine Vibrio harveyi. J Ind Microbiol Biotechnol 38:265–273CrossRefGoogle Scholar
  103. Murugappan RM, Karthikeyan M, Aravinth A, Alamelu MR (2012) Siderophore-mediated iron uptake promotes yeast-bacterial symbiosis. Appl Biochem Biotechnol 168:2170–2183CrossRefGoogle Scholar
  104. Nagoba B, Vedpathak D (2011) Medical applications of siderophores. Eur J Gen Med 8:229–235Google Scholar
  105. Nair A, Juwarkar AA, Singh SK (2007) Production and characterization of siderophores and its application in arsenic removal from contaminated soil. Water Air Soil Pollut 180:199–212CrossRefGoogle Scholar
  106. Nakouti I, Sihanonth P, Palaga T, Hobbs G (2013) Effect of a siderophore producer on animal cell apoptosis: a possible role as anti-cancer agentGoogle Scholar
  107. Neilands JB (1973) Microbial iron transport compounds (siderochromes). Inorg Biochem 1:167–202Google Scholar
  108. Neilands JB (1981) Microbial iron compounds. Annu Rev Biochem 50:715–731CrossRefGoogle Scholar
  109. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726CrossRefGoogle Scholar
  110. Neubauer U, Nowak B, Furrer G, Schulin R (2000) Heavy metal sorption on clay minerals affected by the siderophore desferroixamine B. Environ Sci Technol 34:2749–2755CrossRefGoogle Scholar
  111. Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) Ton B-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64:43–60CrossRefGoogle Scholar
  112. O’Brien S, Hodgson DJ, Buckling A (2014) Social evolution of toxic metal bioremediation in Pseudomonas aeruginosa. Proc R Soc B Biol Sci 281(1787):20140858CrossRefGoogle Scholar
  113. Omidvari M, Sharifi R, Ahmadzadeh M, Dahaji P (2010) Role of fluorescent pseudomonads siderophore to increase bean growth factors. J Agric Sci, N Am 2(3)Google Scholar
  114. Orcutt KM, Jones WS, McDonald A, Schrock D, Wallace KJ (2010) A lanthanide-based chemosensor for bioavailable Fe3+ using a fluorescent siderophore: an assay displacement approach. Sensors (Basel Switzerland) 10(2):1326–1337CrossRefGoogle Scholar
  115. Pal RB, Gokarn K (2010) Siderophores and pathogenecity of microorganisms. J Biosci Technol 1(3):127–134Google Scholar
  116. Pal KK, Tilak KV, Saxena AK, Dey R, Singh CS (2001) Suppression of maize root diseases caused by Macrophomina Phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting Rhizobacteria. Microbiol Res 156:209–223CrossRefGoogle Scholar
  117. Palanche BP, Marmolle F, Abraham MA, Shanzer A, Albrecht-Gray AM (1999) Fluorescent siderophore-based chemosensors: iron (III) quantitative determinations. J Biol Inorg Chem 4:188–198CrossRefGoogle Scholar
  118. Peek ME, Bhatnagar A, McCarty NA, Zughaier SM (2012) Pyoverdine, the major siderophore in Pseudomonas aeruginosa, evades NGAL recognition. Inter disciplinary perspectives on infectious diseases 2012Google Scholar
  119. Perez-Miranda S, Cabirol N, George-Tellez R, Zamudio-Rivera LS, Fernandez FJ (2007) O-CAS, a fast and universal method for siderophore detection. J Microbiol Methods 70:127–131CrossRefGoogle Scholar
  120. Pesce AJ, Kaplan LA (1990) MPtodosQubnicuClinica. Medica Panamericana Ed, Buenos AiresGoogle Scholar
  121. Pietrangelo A (2002) Mechanism of iron toxicity. In: Hershko C (ed) Iron chelation theraphy, Kluwer Academic / Plenum Publishers, New York Vol. 509, 1 Ed pp 19–43Google Scholar
  122. Pogglitsch H, Petek W, Wawschinck O, Holzer W (1981) Treatment of early stages of dialysis encephalopathy by aluminium. Lancet 2:1344–1345CrossRefGoogle Scholar
  123. Poole K, McKay GA (2003) Iron acquisition and its control in Pseudomonas aeruginosa: many roads lead to Rome. Front Biosci 8:d661–d686CrossRefGoogle Scholar
  124. Pramanik A, Braun V (2006) Albomycin uptake via a ferric hydroxamate transport system of Streptococcus pneumoniae R6. J Bacteriol 188(11):3878–3886CrossRefGoogle Scholar
  125. Prashant DS, Makarand RR, Bhushan LC, Sudhir BC (2009) Siderophoregenic Acinetobacter calcoaceticus isolated from wheat rhizosphere with strong PGPR activity. Malays J Microbiol 5:6–12Google Scholar
  126. Propper RD, Cooper B, Rufo RR, Nienhuis AW, Anderson WF, Bunn F, Rosenthal A, Nathan DG (1977) Continuous subcutaneous administration of deferoxamine in patients with iron overload. N Engl J Med 297:418–423CrossRefGoogle Scholar
  127. Qi W, Zhao L (2013) Study of the siderophore producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J Basic Microbiol 53(4):355–364CrossRefGoogle Scholar
  128. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149CrossRefGoogle Scholar
  129. Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394CrossRefGoogle Scholar
  130. Rautio J, Kumpulainen H, Heimbach T, Oliyai R, Oh D, Jarvinen T, Savolainen J (2008) Pro drugs: design and clinical applications. Nat Rev Drug Discov 7:255–270CrossRefGoogle Scholar
  131. Renshaw JC, Robson GD, Trinci AP, Wiebe MG, Livens FR, Collison D, Taylor RJ (2002) Fungal siderophores: structures, functions and applications. Mycol Res 106(10):1123–1142CrossRefGoogle Scholar
  132. Richmond HG (1959) Induction of sarcoma in the rat by iron-dextran complex. Br Med J 1:947CrossRefGoogle Scholar
  133. Robotham JL, Lietman PS (1980) Acute iron poisoning - a review. Am J Dis Child 134:875–897CrossRefGoogle Scholar
  134. Rungin S, Indananda C, Suttiviriya P, Kruasuwan W, Jaemsaeng R, Thamchaipenet A (2012) Plant growth enhancing effects by a siderophore-producing endophytic streptomycete isolated from a Thai jasmine rice plant (Oryza sativa L. cv. KDML105). Antonie Van Leeuwenhoek 102(3):463–472CrossRefGoogle Scholar
  135. Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30Google Scholar
  136. Sayer JM, Emery TF (1968) Structures of the naturally occurring hydroxamic acids, fusarinines A and B. Biochemistry 7:184–190CrossRefGoogle Scholar
  137. Sayyed RZ, Badgujar MD, Sonawane HM, Mhaske MM, Chincholkar SB (2005) Production of microbial iron chelators (siderophores) by fluorescent Pseudomonads. Indian J Biotechnol 4:484–490Google Scholar
  138. Schippers B, Bakker AW, Bakker PA (1987) Interactions of deleterious and beneficial rhizosphere microorganisms and the effect of cropping practices. Ann Rev Phytopathol 25:339–358CrossRefGoogle Scholar
  139. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56CrossRefGoogle Scholar
  140. Seuk C, Paulita T, Baker R (1988) Attributes associate with increased biocontrol activity of fluorescent Pseudomonads. J Plant Pathol 4:218–225Google Scholar
  141. Shenker M, Oliver I, Helmann M, Hadar Y, Chen Y (1992) Utilization by tomatoes of iron mediated by a siderophore produced by Rhizopus arrhizus. J Plant Nutr 15(10):2173–2182CrossRefGoogle Scholar
  142. Simpson LM, Oliver JD (1983) Siderophore production by Vibrio vulnificus. Infect Immun 41:644–649Google Scholar
  143. Smith MJ, Neilands JB (1984) Rhizobactin, a siderophore from Rhizobium meliloti. J Plant Nutr 7:449–458CrossRefGoogle Scholar
  144. Staley JT, Konopka A (1985) Measurement of in situ activities of non photosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346CrossRefGoogle Scholar
  145. Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160CrossRefGoogle Scholar
  146. Sullivan TS, Ramkissoon S, GarrisonVH RA, Thies JE (2012) Siderophore production of African dust microorganisms over Trinidad and Tobago. Aerobiologia 28:391–401CrossRefGoogle Scholar
  147. Summers MR, Jacobs A, Tudway D, Perera P, Rickets C (1979) Studies in desfferoxamine and ferrioxamine metabolism in normal and iron loaded subjects. Br J Haematol 42:547–555CrossRefGoogle Scholar
  148. Taylor KG, Konhauser KO (2011) Iron in earth surface systems. Elements 7:83–120CrossRefGoogle Scholar
  149. Thevenot DR, Toth K, Durst RA, Wilson GS (1999) Electrochemical biosensors: recommended definitions and classification. Pure Appl Chem 71(12):2333–2348CrossRefGoogle Scholar
  150. Thieken A, Winkelmann G (1992) Rhizoferrin: a complexone type siderophore of the mucorales and entomophthorales (Zygomycetes). FEMS Microbiol Lett 94:37–41CrossRefGoogle Scholar
  151. Tian F, Ding Y, Zhu H, Yao L, Du B (2009) Genetic diversity of siderophore-producing bacteria of tobacco rhizosphere. Braz J Microbiol 40:276–284CrossRefGoogle Scholar
  152. Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5(3):240–245CrossRefGoogle Scholar
  153. Toyokuni S (2009) Role of iron in carcinogenesis: cancer as a ferrotoxic disease. Cancer Sci 100:9–16CrossRefGoogle Scholar
  154. Tsafack A, Libman J, Shanzer A, Cabantchik ZI (1996) Chemical determinants of antimalarial activity of reversed siderophores. Antimicrob Agents Chemother 40:2160–2166Google Scholar
  155. Vala AK, Vaidya SY, Dube HC (2000) Siderophore production by facultative marine fungi. Indian J Mar Sci 29:339–340Google Scholar
  156. Vala AK, Dave BP, Dube HC (2006) Chemical characterization and quantification of siderophores produced by marine and terrestrial Aspergilli. Can J Microbiol 52:603–607CrossRefGoogle Scholar
  157. Valco M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208CrossRefGoogle Scholar
  158. Van Scholl L, Kuyper TW, Smits MM, Landeweert R, Hoffland E, van Breemen N (2008) Rock-eating mycorrhizas: their role in plant nutrition and biogeochemical cycles. Plant Soil 303:35–47CrossRefGoogle Scholar
  159. Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiol Lett 309(1):1–7Google Scholar
  160. Vaughn CB, Weinstein R, Bond B, Rice R, Vaughn RW, McKendrick A, Ayad G, Rockwell MA, Rocchio R (1987) Ferritin content in human cancerous and noncancerous colonic tissue. Cancer Invest 5:7–10CrossRefGoogle Scholar
  161. Velasquez IB (2011) Characterization of siderophores in the Southern Ocean. Ph. D. thesis, University of Otago, Dunedin, New ZealandGoogle Scholar
  162. Verma VC, Singh SK, Prakash S (2011) Bio-control and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachtaindica A. Juss. J Basic Microbiol 51:550–556CrossRefGoogle Scholar
  163. Voisard C, Keel C, Haas D, Defago G (1989) Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J 8(2):351–358Google Scholar
  164. Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647CrossRefGoogle Scholar
  165. Wang Q, Xiong D, Zhao P, Yu X, Tu B, Wang G (2011) Effect of applying an arsenic-resistant and plant growth-promoting Rhizobacterium to enhance soil arsenic phyto-remediation by Populusdeltoides LH05-17. J Appl Microbiol 111:1065–1074CrossRefGoogle Scholar
  166. Wichard T, Bellenger JP, Morel FM, Kraepiel AM (2009) Role of the siderophore azotobactin in the bacterial acquisition of nitrogenase metal cofactors. Environ Sci Technol 43:7218–7224CrossRefGoogle Scholar
  167. Wilson MK, Abergel RJ, Raymond KN, Arceneaux JE, Byers BR (2006) Siderophores of Bacillus anthracis, Bacillus cereus and Bacillus thuringiensis. Biochem Biophys Res Commun 348:320–325CrossRefGoogle Scholar
  168. Winkelman G, Drechsel H (1997) Microbial siderophores. In: Kleinkauf H, von Dohren H (eds) Products of secondary metabolism, Vol 7. Wiley VCH, Germany, Weinheim 200–46Google Scholar
  169. Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392CrossRefGoogle Scholar
  170. Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN EcolGoogle Scholar
  171. Yadav S, Kaushik R, Saxena AK, Arora DK (2011) Diversity and phylogeny of plant growth-promoting bacilli from moderately acidic soil. J Basic Microbiol 51:98–106CrossRefGoogle Scholar
  172. Yamaguchi K, Mandai M, Toyokuni S, Hamanishi J, Higuchi T, Takakura K, Fujii S (2008) Contents of endometriotic cysts, especially the high concentration of free iron, are a possible cause of carcinogenesis in the cysts through the iron-induced persistent oxidative stress. Clin Cancer Res 14:32–40CrossRefGoogle Scholar
  173. Yang X, Baligar VC, Martens DC, Clark PB (1996) Plant tolerance to nickel toxicity. II. Nickel effect on influx and transport of mineral nutrients in four plant species. J Plant Nutr 19(2):265–279CrossRefGoogle Scholar
  174. Yu X, Ai C, Xin L, Zhou G (2011) The siderophore producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur J Soil Biol 47:138–145CrossRefGoogle Scholar
  175. Zacharski LR, Chow BK, Howes PS, Shamayeva G, Baron JA, Dalman RL, MalenkaDJ OCK, Lavori PW (2008) Decreased cancer risk after iron reduction in patients with peripheral arterial disease: results from a randomized trial. J Natl Cancer Inst 100:996–1002CrossRefGoogle Scholar
  176. Zahner H, Keller-Schierlein W, Hutter R, Hess-Leisinger K, Deer A (1963) Stoffwechselprodukte von Mikroorganismen 40. Mitteilung. SideramineausAspergillaceen. Arch Microbiol 45:119–135Google Scholar
  177. Zhang MK, Liu ZY, Wang H (2010) Use of single extraction methods to predict bioavailability of heavy metals in polluted soils to rice. Commun Soil Sci Plant Anal 41(7):820–831CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Maumita Saha
    • 1
  • Subhasis Sarkar
    • 1
  • Biplab Sarkar
    • 3
  • Bipin Kumar Sharma
    • 2
  • Surajit Bhattacharjee
    • 1
  • Prosun Tribedi
    • 2
  1. 1.Department of Molecular Biology & BioinformaticsTripura University (A Central University)SuryamaninagarIndia
  2. 2.Department of MicrobiologyTripura University (A Central University)SuryamaninagarIndia
  3. 3.National Institute of Abiotic Stress ManagementPuneIndia

Personalised recommendations