Skip to main content

Advertisement

Springer Nature Link
Log in

Microbial siderophores and their potential applications: a review

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • Ackrill P, Raiston AJ, Day JP, Hoodge KC (1980) Successful removal of aluminum from patients with encephalopathy. Lancet 2:692–693

    Article  CAS  Google Scholar 

  • Ahmed E, Holmstrom SJM (2014) Siderophores in environmental research: roles and applications. Microb Biotechnol 7:196–208

    Article  CAS  Google Scholar 

  • Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by Rhizosphere bacteria. Biol Fertil Soils 12:39–45

    Article  CAS  Google Scholar 

  • Ali SS, Vidhale NN (2013) Bacterial siderophore and their application: a review. Int J Curr Microbiol Appl Sci 2:303–312

    Google Scholar 

  • Arze RS, Parkinson IS, Cartilidge NEF, Britton P, Ward MK (1981) Reversal of aluminium dialysis encephalopathy after desferrioxamine treatment. Lancet 318(8255):1116

    Article  Google Scholar 

  • 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):1069–1078

    Article  CAS  Google Scholar 

  • Barrero JM, Moreno-Bondi MC, Perez-Conde MC, Camara C (1993) A biosensor for ferric ion. Talanta 40(11):1619–1623

    Article  CAS  Google Scholar 

  • 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 79:2345–2355

    Article  CAS  Google Scholar 

  • Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting Rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051

    Article  CAS  Google Scholar 

  • Bingham FT, Pereyea FJ, Jarrell WM (1986) Metal toxicity to agricultural crops. Met Ions Biol Syst 20:119–156

    CAS  Google Scholar 

  • Blatt J, Stitely S (1987) Antineuroblastoma activity of desferoxamine in human cell lines. Cancer Res 47:1749–1750

    CAS  Google Scholar 

  • Blatt J, Taylor SR, Stitely S (1988) Mechanism of antineuroblastoma activity of deferoxamine in vitro. J Lab Clin Med 112:433–436

    CAS  Google Scholar 

  • Bollard EG (1983) Involvement of unusual elements in plant growth and nutrition. Encyclopedia of plant physiology. New series

  • Bou-Abdallah F (2010) The iron redox and hydrolysis chemistry of the ferritins. Biochim Biophys Acta Gen Subj 1800(8):719–731

    Article  CAS  Google Scholar 

  • 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 Laboratory

  • 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 11:1079–1091

    Article  CAS  Google Scholar 

  • 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 74:280–286

    Article  CAS  Google Scholar 

  • Braun V, Pramanik A, Gwinner T, Koberle M, Bohn E (2009) Sideromycins: tools and antibiotics. BioMetals 22:3–13

    Article  CAS  Google Scholar 

  • 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 84:69–81

    Article  CAS  Google Scholar 

  • Brinton LA, Gridley G, Persson I, Baron J, Bergqvist A (1997) Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol 176:572–579

    Article  CAS  Google Scholar 

  • 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 36:2166–2175

    Article  CAS  Google Scholar 

  • Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245

    Article  CAS  Google Scholar 

  • Burt WR, Underwood AL, Appleton GL (1981) Hydroxamic acid from Histoplasma capsulatum that displays growth factor activity. Appl Environ Microbiol 42:560–563

    CAS  Google Scholar 

  • Buss JL, Torti FM, Torti SV (2003) The role of iron chelation in cancer therapy. Curr Med Chem 10:1021–1034

    Article  CAS  Google Scholar 

  • 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 164:570–577

    Article  CAS  Google Scholar 

  • 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):37–41

    Article  Google Scholar 

  • 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):275

    Article  CAS  Google Scholar 

  • 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 61:414–423

    Article  CAS  Google Scholar 

  • Carson JK, Campbell L, Rooney D, Clipson N, Gleeson DB (2009) Minerals in soil select distinct bacterial communities in their microhabitats. FEMS Microbiol Ecol 67:381–388

    Article  CAS  Google Scholar 

  • 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: Springer

  • 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 270:1689–1698

    Article  CAS  Google Scholar 

  • 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 78:5040–5045

    Article  CAS  Google Scholar 

  • 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 69:4706–4713

    Article  CAS  Google Scholar 

  • 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 169–189

    Chapter  Google Scholar 

  • 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 17:254–264

    Article  CAS  Google Scholar 

  • Dave BP, Dube HC (2000) Chemical characterization of fungal siderophores. Indian J Exp Biol 38:56–62

    CAS  Google Scholar 

  • Dave BP, Anshuman K, Hajela P (2006) Siderophores of halophilic archaea and their chemical characterization. Indian J Exp Biol 44:340–344

    CAS  Google Scholar 

  • Dertz EA, Xu J, Stintzi A, Raymond KN (2006) Bacillibactin-mediated iron transport in Bacillus subtilis. J Am Chem Soc 128:22–23

    Article  CAS  Google Scholar 

  • Diekmann H, Zahner H (1967) Konstitution von Fusigen und dessen Abbau zu Δ2‐Anhydromevalonsaurelacton. Eur J Biochem 3(2):213–218

    Article  CAS  Google Scholar 

  • 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 14:105–112

    Article  CAS  Google Scholar 

  • 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 8:278–292

    Article  CAS  Google Scholar 

  • Eggins BR (1996) Biosensors: an introduction. Wiley, Chichester, UK, pp 16–19

  • 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):11–22

    Article  CAS  Google Scholar 

  • 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):5228–5233

    CAS  Google Scholar 

  • 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):5857–5864

    Article  CAS  Google Scholar 

  • 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. 695–705

  • 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 196:147–151

    Article  CAS  Google Scholar 

  • Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress and antioxidant nutrients. Toxicology 189:147–163

    Article  CAS  Google Scholar 

  • Gamalero E, Glick BR (2011) Mechanisms used by plant growth-promoting bacteria. In Bacteria in Agrobiology: Plant Nutrient Management. Springer Berlin Heidelberg, 17–46

  • Gamit DA, Tank SK (2014) Effect of siderophore producing microorganism on plant growth of Cajanus cajan (Pigeon pea). Int J Res Pure Appl Microbiol 4:20–27

    Google Scholar 

  • Gangwar M, Kaur G (2009) Isolation and characterization of endophytic bacteria from endorhizosphere of sugarcane and ryegrass. Internet J Microbiol 7:139–144

    Google Scholar 

  • Gledhill M (2001) Electrospray ionisation-mass spectrometry of hydroxamate siderophores. Analyst 126(8):1359–1362

    Article  CAS  Google Scholar 

  • 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):2973–2980

    Article  CAS  Google Scholar 

  • Gorska A, Sloderbach A, Marszall MP (2014) Siderophore-drug complexes: potential medicinal applications of the ‘Trojan horse’ strategy. Trends Pharmacol Sci 35(9):442–449

    Article  CAS  Google Scholar 

  • Griffiths GL, Sigel SP, Payne SM, Neilands JB (1984) Vibriobactin, a siderophore from Vibrio cholerae. J Biol Chem 259(1):383–385

    CAS  Google Scholar 

  • Guan LL, Kamino K (2001) Bacterial response to siderophore and quorum-sensing chemical signals in the seawater microbial community. BMC Microbiol 1(1):27

    Article  CAS  Google Scholar 

  • 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):284–296

    Article  CAS  Google Scholar 

  • 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 206:605–609

    Article  CAS  Google Scholar 

  • Gysin J, Crenn Y, Pereira Da Silva L, Breton C (1991) Siderophores as anti parasitic agents. US Patent (US 5192807 A) 5:192–807

    Google Scholar 

  • 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 57:3270–3277

    CAS  Google Scholar 

  • 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 50:195–202

    Article  CAS  Google Scholar 

  • 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 100:3677–3682

    Article  CAS  Google Scholar 

  • He ZL, Yang XE (2007) Role of soil rhizobacteria in phytoremediation of heavy metal contaminated soils. J Zhejiang Univ Sci B 8(3):192–207

    Article  CAS  Google Scholar 

  • 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 50:1251–1257

    CAS  Google Scholar 

  • 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 77–89

  • Hofte M (1993) Classes of microbial siderophores. Iron chelation in plants and soil microorganisms. Academic Press Inc 3–26

  • Holinsworth B, Martin JD (2009) Siderophore production by marine-derived fungi. BioMetals 22(4):625–632

    Article  CAS  Google Scholar 

  • Holzberg M, Artis WM (1983) Hydroxamate siderophore production by opportunistic and systemic fungal pathogens. Infect Immun 40:1134–1139

    CAS  Google Scholar 

  • 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):1299–1315

    Article  CAS  Google Scholar 

  • Huber DL (2005) Synthesis, properties, and applications of iron nanoparticles. Small 1(5):482–501

    Article  CAS  Google Scholar 

  • 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):143–151

    Article  Google Scholar 

  • 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 071

  • 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):7–18

    Article  CAS  Google Scholar 

  • 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 9:40–51

    Article  CAS  Google Scholar 

  • Kaeberlein T, Lewis K, Epstein SS (2002) Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:1127–1129

    Article  CAS  Google Scholar 

  • Kannahi M, Senbagam N (2014) Studies on siderophore production by microbial isolates obtained from rhizosphere soil and its antibacterial activity. J Chem Pharm Res 6:1142–1145

    CAS  Google Scholar 

  • Keller M, Zengler K (2004) Tapping into microbial diversity. Nat Rev Microbiol 2:141–150

    Article  CAS  Google Scholar 

  • 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):490–496

    CAS  Google Scholar 

  • 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 4:437

    Article  CAS  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schiroth MN (1980) Enhanced plant growth by siderophores produced by plant growth promoting Rhizobacteria. Nature 286:885–886

    Article  CAS  Google Scholar 

  • Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci 66:3–18

    Article  CAS  Google Scholar 

  • Krewulak KD, Vogel HJ (2008) Structural biology of bacterial iron uptake. Biochim Biophys Acta Biomembr 1778(9):1781–1804

    Article  CAS  Google Scholar 

  • 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):521–528

    Article  Google Scholar 

  • 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):18–31

    Article  CAS  Google Scholar 

  • Leong SA, Neilands JB (1982) Siderophore production by phytopathogenic microbial species. Arch Biochem Biophys 281:351–359

    Article  Google Scholar 

  • Lewis K, Epstein S, D’Onofrio A, Ling LL (2010) Uncultured microorganisms as a source of secondary metabolites. J Antibiot 63(8):468–476

    Article  CAS  Google Scholar 

  • Lovejoy DB, Richardson DR (2003) Iron chelators as anti-neoplastic agents: current developments and promise of the PIH class of chelators. Cur Med Chem 10:1035–1049

    Article  CAS  Google Scholar 

  • 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 91:218–224

    Article  CAS  Google Scholar 

  • 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 101:43–59

    Article  CAS  Google Scholar 

  • Marschner H, Romheld V, Kissel M (1986) Different strategies in higher plants in mobilization and uptake of iron. J Plant Nutr 9:695–713

    Article  CAS  Google Scholar 

  • 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 30:433–439

    Article  CAS  Google Scholar 

  • 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 43:8538–8546

    Article  CAS  Google Scholar 

  • Maurer B, Keller-Schierlein W (1968) Ferribactin, a Siderochrome from Pseudomonas fluorescens Migula: 61. Mitteilung Ferribactin, ein Siderochromaus Pseudomonas fluorescens Migula. Arch Microbiol 60:326–339

    CAS  Google Scholar 

  • 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 276:7209–7217

    Article  CAS  Google Scholar 

  • 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):2647–2652

    Article  CAS  Google Scholar 

  • 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):1760–1763

    CAS  Google Scholar 

  • 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 67:201–206

    Article  CAS  Google Scholar 

  • Messenger AJ, Barclay R (1983) Bacteria, iron and pathogenicity. Biochem Educ 11(2):54–63

    Article  CAS  Google Scholar 

  • Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451

    Article  CAS  Google Scholar 

  • 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):3461–3468

    Article  CAS  Google Scholar 

  • 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):615–624

    Article  CAS  Google Scholar 

  • Murugappan RM, Aravinth A, Karthikeyan M (2011) Chemical and structural characterization of hydroxamate siderophore produced by marine Vibrio harveyi. J Ind Microbiol Biotechnol 38:265–273

    Article  CAS  Google Scholar 

  • Murugappan RM, Karthikeyan M, Aravinth A, Alamelu MR (2012) Siderophore-mediated iron uptake promotes yeast-bacterial symbiosis. Appl Biochem Biotechnol 168:2170–2183

    Article  CAS  Google Scholar 

  • Nagoba B, Vedpathak D (2011) Medical applications of siderophores. Eur J Gen Med 8:229–235

    Google Scholar 

  • 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 180:199–212

    Article  CAS  Google Scholar 

  • Nakouti I, Sihanonth P, Palaga T, Hobbs G (2013) Effect of a siderophore producer on animal cell apoptosis: a possible role as anti-cancer agent

  • Neilands JB (1973) Microbial iron transport compounds (siderochromes). Inorg Biochem 1:167–202

    CAS  Google Scholar 

  • Neilands JB (1981) Microbial iron compounds. Annu Rev Biochem 50:715–731

    Article  CAS  Google Scholar 

  • Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726

    Article  CAS  Google Scholar 

  • Neubauer U, Nowak B, Furrer G, Schulin R (2000) Heavy metal sorption on clay minerals affected by the siderophore desferroixamine B. Environ Sci Technol 34:2749–2755

    Article  CAS  Google Scholar 

  • Noinaj N, Guillier M, Barnard TJ, Buchanan SK (2010) Ton B-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 64:43–60

    Article  CAS  Google Scholar 

  • 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):20140858

    Article  CAS  Google Scholar 

  • 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)

  • 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):1326–1337

    Article  CAS  Google Scholar 

  • Pal RB, Gokarn K (2010) Siderophores and pathogenecity of microorganisms. J Biosci Technol 1(3):127–134

    Google Scholar 

  • 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 156:209–223

    Article  CAS  Google Scholar 

  • Palanche BP, Marmolle F, Abraham MA, Shanzer A, Albrecht-Gray AM (1999) Fluorescent siderophore-based chemosensors: iron (III) quantitative determinations. J Biol Inorg Chem 4:188–198

    Article  CAS  Google Scholar 

  • 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 2012

  • 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 70:127–131

    Article  CAS  Google Scholar 

  • Pesce AJ, Kaplan LA (1990) MPtodosQubnicuClinica. Medica Panamericana Ed, Buenos Aires

    Google Scholar 

  • 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 19–43

  • Pogglitsch H, Petek W, Wawschinck O, Holzer W (1981) Treatment of early stages of dialysis encephalopathy by aluminium. Lancet 2:1344–1345

    Article  CAS  Google Scholar 

  • Poole K, McKay GA (2003) Iron acquisition and its control in Pseudomonas aeruginosa: many roads lead to Rome. Front Biosci 8:d661–d686

    Article  CAS  Google Scholar 

  • Pramanik A, Braun V (2006) Albomycin uptake via a ferric hydroxamate transport system of Streptococcus pneumoniae R6. J Bacteriol 188(11):3878–3886

    Article  CAS  Google Scholar 

  • Prashant DS, Makarand RR, Bhushan LC, Sudhir BC (2009) Siderophoregenic Acinetobacter calcoaceticus isolated from wheat rhizosphere with strong PGPR activity. Malays J Microbiol 5:6–12

    Google Scholar 

  • 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 297:418–423

    Article  CAS  Google Scholar 

  • 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):355–364

    Article  CAS  Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149

    Article  CAS  Google Scholar 

  • Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394

    Article  CAS  Google Scholar 

  • 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 7:255–270

    Article  CAS  Google Scholar 

  • 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):1123–1142

    Article  CAS  Google Scholar 

  • Richmond HG (1959) Induction of sarcoma in the rat by iron-dextran complex. Br Med J 1:947

    Article  CAS  Google Scholar 

  • Robotham JL, Lietman PS (1980) Acute iron poisoning - a review. Am J Dis Child 134:875–897

    Article  CAS  Google Scholar 

  • 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):463–472

    Article  CAS  Google Scholar 

  • Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30

    Google Scholar 

  • Sayer JM, Emery TF (1968) Structures of the naturally occurring hydroxamic acids, fusarinines A and B. Biochemistry 7:184–190

    Article  CAS  Google Scholar 

  • Sayyed RZ, Badgujar MD, Sonawane HM, Mhaske MM, Chincholkar SB (2005) Production of microbial iron chelators (siderophores) by fluorescent Pseudomonads. Indian J Biotechnol 4:484–490

    CAS  Google Scholar 

  • Schippers B, Bakker AW, Bakker PA (1987) Interactions of deleterious and beneficial rhizosphere microorganisms and the effect of cropping practices. Ann Rev Phytopathol 25:339–358

    Article  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  Google Scholar 

  • Seuk C, Paulita T, Baker R (1988) Attributes associate with increased biocontrol activity of fluorescent Pseudomonads. J Plant Pathol 4:218–225

    Google Scholar 

  • 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):2173–2182

    Article  CAS  Google Scholar 

  • Simpson LM, Oliver JD (1983) Siderophore production by Vibrio vulnificus. Infect Immun 41:644–649

    CAS  Google Scholar 

  • Smith MJ, Neilands JB (1984) Rhizobactin, a siderophore from Rhizobium meliloti. J Plant Nutr 7:449–458

    Article  CAS  Google Scholar 

  • Staley JT, Konopka A (1985) Measurement of in situ activities of non photosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39:321–346

    Article  CAS  Google Scholar 

  • Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194:4151–4160

    Article  CAS  Google Scholar 

  • Sullivan TS, Ramkissoon S, GarrisonVH RA, Thies JE (2012) Siderophore production of African dust microorganisms over Trinidad and Tobago. Aerobiologia 28:391–401

    Article  Google Scholar 

  • 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 42:547–555

    Article  CAS  Google Scholar 

  • Taylor KG, Konhauser KO (2011) Iron in earth surface systems. Elements 7:83–120

    Article  CAS  Google Scholar 

  • Thevenot DR, Toth K, Durst RA, Wilson GS (1999) Electrochemical biosensors: recommended definitions and classification. Pure Appl Chem 71(12):2333–2348

    Article  CAS  Google Scholar 

  • Thieken A, Winkelmann G (1992) Rhizoferrin: a complexone type siderophore of the mucorales and entomophthorales (Zygomycetes). FEMS Microbiol Lett 94:37–41

    Article  CAS  Google Scholar 

  • Tian F, Ding Y, Zhu H, Yao L, Du B (2009) Genetic diversity of siderophore-producing bacteria of tobacco rhizosphere. Braz J Microbiol 40:276–284

    Article  Google Scholar 

  • Torsvik V, Ovreas L (2002) Microbial diversity and function in soil: from genes to ecosystems. Curr Opin Microbiol 5(3):240–245

    Article  CAS  Google Scholar 

  • Toyokuni S (2009) Role of iron in carcinogenesis: cancer as a ferrotoxic disease. Cancer Sci 100:9–16

    Article  CAS  Google Scholar 

  • Tsafack A, Libman J, Shanzer A, Cabantchik ZI (1996) Chemical determinants of antimalarial activity of reversed siderophores. Antimicrob Agents Chemother 40:2160–2166

    CAS  Google Scholar 

  • Vala AK, Vaidya SY, Dube HC (2000) Siderophore production by facultative marine fungi. Indian J Mar Sci 29:339–340

    Google Scholar 

  • Vala AK, Dave BP, Dube HC (2006) Chemical characterization and quantification of siderophores produced by marine and terrestrial Aspergilli. Can J Microbiol 52:603–607

    Article  CAS  Google Scholar 

  • Valco M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208

    Article  Google Scholar 

  • 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 303:35–47

    Article  CAS  Google Scholar 

  • Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiol Lett 309(1):1–7

    CAS  Google Scholar 

  • 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 5:7–10

    Article  CAS  Google Scholar 

  • Velasquez IB (2011) Characterization of siderophores in the Southern Ocean. Ph. D. thesis, University of Otago, Dunedin, New Zealand

  • 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 51:550–556

    Article  CAS  Google Scholar 

  • 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):351–358

    CAS  Google Scholar 

  • Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647

    Article  CAS  Google Scholar 

  • 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 111:1065–1074

    Article  CAS  Google Scholar 

  • 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 43:7218–7224

    Article  CAS  Google Scholar 

  • Wilson MK, Abergel RJ, Raymond KN, Arceneaux JE, Byers BR (2006) Siderophores of Bacillus anthracis, Bacillus cereus and Bacillus thuringiensis. Biochem Biophys Res Commun 348:320–325

    Article  CAS  Google Scholar 

  • Winkelman G, Drechsel H (1997) Microbial siderophores. In: Kleinkauf H, von Dohren H (eds) Products of secondary metabolism, Vol 7. Wiley VCH, Germany, Weinheim 200–46

  • Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392

    Article  CAS  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol

  • Yadav S, Kaushik R, Saxena AK, Arora DK (2011) Diversity and phylogeny of plant growth-promoting bacilli from moderately acidic soil. J Basic Microbiol 51:98–106

    Article  CAS  Google Scholar 

  • 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 14:32–40

    Article  CAS  Google Scholar 

  • 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):265–279

    Article  CAS  Google Scholar 

  • 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 47:138–145

    Article  Google Scholar 

  • 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 100:996–1002

    Article  CAS  Google Scholar 

  • Zahner H, Keller-Schierlein W, Hutter R, Hess-Leisinger K, Deer A (1963) Stoffwechselprodukte von Mikroorganismen 40. Mitteilung. SideramineausAspergillaceen. Arch Microbiol 45:119–135

    Google Scholar 

  • 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):820–831

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Molecular Biology & Bioinformatics, Tripura University (A Central University), Suryamaninagar, Tripura, 799022, India

    Maumita Saha, Subhasis Sarkar & Surajit Bhattacharjee

  2. Department of Microbiology, Tripura University (A Central University), Suryamaninagar, Tripura, 799022, India

    Bipin Kumar Sharma & Prosun Tribedi

  3. National Institute of Abiotic Stress Management, Baramati, 413115, Pune, Maharashtra, India

    Biplab Sarkar

Authors
  1. Maumita Saha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Subhasis Sarkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Biplab Sarkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bipin Kumar Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Surajit Bhattacharjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Prosun Tribedi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Surajit Bhattacharjee or Prosun Tribedi.

Additional information

Responsible editor: Robert Duran

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saha, M., Sarkar, S., Sarkar, B. et al. Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res 23, 3984–3999 (2016). https://doi.org/10.1007/s11356-015-4294-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4294-0

Keywords

Search

Navigation