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Siderophore: Structural and Functional Characterisation – a Comprehensive Review

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Siderophore: Structural and Functional Characterisation – a Comprehensive Review Agriculture (Poľnohospodárstvo), 61, 2015 (3): 97−114 DOI: 10.1515/agri-2015-0015 REVIEW SIDEROPHORE: STRUCTURAL AND FUNCTIONAL CHARACTERISATION – A COMPREHENSIVE REVIEW STUTI SAH, RAJNI SINGH* Amity Institute of Microbial biotechnology, Amity University, Uttar Pradesh SAH, S. ‒ SINGH, R.: Siderophore: structural and functional characterisation ‒ a comprehensive review. Agriculture (Poľnohospodárstvo), vol. 61, 2015, no. 3, pp. 97–114. Plants and microbes have enormous importance in our with iron across the memberane and depending on the daily life. Iron is said to be the fourth most abundant difference in their chemical structure, functional moiety element in the earth's crust from soil, still many plants and their source of isolation of four different types of si- face problem in uptaking iron because it is found in in- derophore (hydroxamates, catecholates, carboxylates and soluble form, which severely restricts the bioavailability siderophore with mixed ligand). Siderophore and their of this metal. In response to this, microorganisms present derivative have large application in agriculture as to in- in soil such as Pseudomonas sp., Enterobacter genera, crease soil fertility and as biocontrol for fungal pathogen. Bacillus and Rhodococcus produce special iron carriers or This review unlike other reviews includes (1) types of iron-binding compounds called as ‘siderphores’ or ‘side- siderophore, (2) the structural difference amongst them, rochromes’. This paper is an attempt to review the impor- (3) siderophore biosynthesis, (4) transport mechanism, tance of siderphores in enhancing plants’ iron utilisation (5) the genetics of siderophore and (6) their efficacy in strategies, the mode of transport of siderophores along human life. Key words: siderophore, phytosiderophore, catecholate siderophore, hydroxamate siderophores, carboxylate siderophore, transport of iron, rhizosphere bacteria Siderophores are compounds from ancient Greek excretion of phytosiderophore (i.e. chelate com- words, sidero ‘iron’ and phore ‘carriers’ meaning pounds, common in grasses that sequester iron) by ‘iron carriers’. These are low-molecular-weight the roots and secretion of siderophore by group of (<10 kDa) iron-chelating compounds, produced by microbes to facilitate the Fe complex uptake under ‘rhizospheric bacteria’ under iron-limited condi- iron deficiency conditions, which binds with high tions in order to enhance the plant growth by scav- affinity for iron (Takagi 1976; Mino et al. 1983; enging iron from the environment and making the Marschner et al. 1986; Neilands 1995; Kannahi & mineral available to the cell near the root (Neilands Senbagam 2014). It has been assumed that compe- 1952; Lankford 1973; Alexander & Zubererm 1991; tition for iron in the rhizosphere is controlled by Hider & Kong 2010; Maheshwari 2011; Ahmed & the empathy of the siderophores for iron (Loper & Holmstrom 2014). Iron is the major component for Henkels 1999; Bernd & Rehm 2008; Munees & Mu- various vital functions (photosynthesis, enzyme co- lugeta 2014). Siderophores function as plant growth factor, redox reagent, respiration, synthesis of nu- promoters (Yadav et al. 2011; Verma et al. 2011), cleosides and amino acids) of the plant. Owing to biocontrol agents (Verma et al. 2011) and bioreme- deficiency of iron, various plants seem to rely on diation agents (Wang et al. 2011; Ishimaru et al. Prof. (Dr.) Rajni Singh (Additional Director) (*Corresponding author), Amity Institute of Microbial Biotechnology, Amity University, Sector 125, Noida,UP, India. E-mail: [email protected]; [email protected] 97 Agriculture (Poľnohospodárstvo), 61, 2015 (3): 97−114 2012), in addition to their valuable role in soil min- go intermolecular cyclisation, yielding enterobac- eral weathering (Reichard et al. 2005; Buss et al. tin. Enterobactin was the first tricatechol sidero- 2007; Shirvani & Nourbakhsh 2010). Alkaline soils phore, isolated from Escherichia coli, Aerobacter are considered to be the potential inducers of iron aerogenes and Salmonella typhimurium (Ward et al. deficiency in plants in spite of the presence of iron 1999). Enterobactin (Enterochelin) are produced by in high concentration in the soil, when the soil pH bacteria of the family Enterobacteriaceae, includes exceeds 6.5–7.0, the availability of iron in the soil is all strains of E. coli having high affinity for iron. significantly reduced, whilst calcareous soils, which S. typhimurium, Klebsiella pneumoniae and Erwinia have high pH, decrease the affinity of plants for Fe herbicola are also known to produce enterobactin. and thus impede Fe uptake mechanism. Enterobactin is the strongest siderophore having the capacity to chelate iron even from the environment Classification of Siderphores where concentration of iron is very low (Raymond A great variation is seen in siderophore structure et al. 2003). E. coli enterobactin has a molecular produced by many bacteria. Siderophores are gener- weight of 669 kDa, which exceeds the size limit ally classified on the basis of co-ordinating groups for diffusion across the outer membrane. Therefore, that chelate the Fe (III) ion. The most common co-or- enterobactin are synthesised with the help of active dinating groups are catecholates, hydroxamates and transport mechanism for transport and capturing carboxylates (Ali & Vidhale 2013). A minority of iron (Hans et al. 2001; Gregory et al. 2012). In the siderophores have chemically distinct Fe (III) ion year 1998, Cornish and Page observed that the cat- binding group, including salicylic acid, oxazoline echolate siderophores were hyper-produced to offer or thizoline nitrogen. Some siderophores including chemical protection from oxidative damage cata- pyoverdines are classified as ‘mixed ligands’ having lysed by O and Fe. co-ordinating groups that fall into chemically differ- 2 ent classes (Table 1). Different types of siderophore 2. Hydroxamate-type siderophores were identified by electrophoretic mobility, spectro- Ferrichrome-type hydroxamate siderophores are photometric titration, proton nuclear magnetic reso- of special ecological interest because of their pro- nance spectroscopy, mass spectrometry, acid hydro- duction by many soil fungi (Zahneret et al. 1963; lysis and biological activity. O’Sulivan & O’Gara 1992; Schalk et al. 2011), in- cluding symbiotic ectomycorrhizal fungi, and their 1. Catecholate – siderophore ability to mobilise iron in neutral and alkaline soils Siderophore exhibiting phenolate or 2,3-dihy- in which other naturally occurring compounds are droxy benzoate (DHB) binding groups belong to ineffective as iron chelators because of competition the catecholate type of siderophore. Catechol, also from other metal ions (Cline et al. 1982). Experi- known as pyrocatechol or 1,2-dihydroxybenzene, is mental evidence indicates that hydroxamate sid- an organic compound with the molecular formula erophores can supply iron to some plant species. C H (OH) . It is the orthoisomer of the three isomer- 6 4 2 Hydroxamate siderophores are generally produced ic benzenediols. This colourless compound occurs by fungi and belong to Zygomycotina (Mucorales), naturally in trace amounts. In iron-limited medium, Ascomycotina (Aspergilli, Penicillia, Neurospora- Azotobacter vinelandii produces three catecholate crassa) and Deuteromycotina (Fusarium dimerum). siderophores, namely, tricatecholate protochelin, Hydroxamate siderophores were mostly trihydrox- the dicatecholate azotochelin and the monocatecho- amates, followed by dihydroxamates. Monohydrox- late aminochelin (Corbin & Bulen 1969; Page & amate nature was not shown by any of the report- Tigerstrom 1988; Cornish & Page 1995; Wittmann ed fungal siderophores. Hydroxamate siderophores et al. 2001). formed hexadentate, tetradentates and bidentate 1.1 Enterobactin ligands. A good correlation was observed between This catecholate-type siderophore is a cyclic tri- hydroxamate groups and ligand property. Ferri- mer composed of 2,3-dihydroxy-N-benzoylserine. chrome belonging to hydroxamate are either linear Three molecules of the DHB-Ser formed under- or crystal in structure. Certain ferrichrome deriva- 98 Agriculture (Poľnohospodárstvo), 61, 2015 (3): 97−114 T a b l e 1 Structural, chemical and functional moiety of major bacterial siderophore Type of Side- Chemical Bacterial Structure Function Reference rophore moiety source 1 Catecholate: phenolate or 2,3-dihydroxy benzoate (DHB) binding groups Pollack & Neilands 1970; 2,3-dihydroxy Walsh et al. 1990; -N-benzoylse- Iron-chelating Family Ente- O'Brien et al. 1970; rine a cyclic compound (a) Enterobactin robacteriaceae, Gregory et al. 2012; trimer and used in e.g. E. coli IUPAC, Commis- agriculture sion on Nomen- clature of Organic Chemistry, 1993 2 Hydroxamate: esters or acid chlorides or carboxylic acids Used medically O'Brien et al. 1970; for the binding Gregory et al. 2012; (a) Aferrioxa- Linear trihyd- of excess blood Streptomyces IUPAC, Commis- mines roxamates iron in the and Nocardia sion on Nomen- treatment of clature of Organic thalsaemia Chemistry, 1993 Jalal & van der Helm 1991; O'Brien Basidomyce- et al. 1970; Gregory Growth factor tes producing Cyclic trihyd- et al. 2012; IUPAC, (b) Ferrichrome for other mic- fungal species, roxamate Commission on robes e.g. Ustilagos- Nomenclature of phaerogena Organic Chemistry, 1993 Buyer et al. 1991; Pseudomonas Meyrier 1999; Sequester iron A trihydroxy- of marine ori- O'Brien et al. 1970; in iron-poor tetraoxo tetra gin, Klebisella Gregory et al. 2012; (c) Aerobactin environments
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