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Marine-Derived Fungal Siderophores: a Perception

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Marine-Derived Fungal Siderophores: a Perception Indian Journal of Geo-Marine Science Vol. 45(3) March 2016, pp. 431-439 Marine-derived Fungal Siderophores: A Perception Hiral B. Trivedi, Anjana K. Vala, Jaykishan H. Dhrangadhriya & Bharti P. Dave* Department of Life Sciences, Maharaja Krishnakumarsinhji Bhavnagar University, Sardar Vallabhbhai Patel Campus, Bhavnagar-364 001, Gujarat, India [E-mail: [email protected]] Received 25August 2014; revised 01 October 2014 Siderophores play crucial role in biogeochemical cycle in terrestrial as well as marine environment. Siderophores of bacteria from marine habitats have been extensively studied, however, comparatively less information is available on their fungal counter parts. This review focuses on siderophores of marine-derived fungi, molecular mechanism of siderophore biosynthesis and their uptake. Their chemical nature and applications are also discussed. Data so far available on marine fungal siderophores are found to be very interesting. Though less explored, the information available reveals novelty in chemical nature of siderophores of marine-derived fungi, i.e. occurrence of catecholates in fungi and carboxylates in non- mucoraceous fungi, which is the first-ever report. Further investigations on marine-derived fungal siderophores would be an interesting area of research. [Key words: Siderophore, Marine-derived fungi, Catecholate, Carboxylate, Hydroxamate] Introduction low iron concentration affecting the primary production. Marine microorganisms affected by Iron is an essential macronutrient for the growth this critical situation cope up with this stressing of microorganisms. It plays crucial role in condition by producing siderophores to gain iron various cellular processes like DNA/RNA in HNLC regions [9-19]. While much work is synthesis, ATP synthesis, respiration and also as done on bacterial siderophores from marine [1] a cofactor of numerous enzymes . Despite its habitats, fungal siderophores have been imperative role in microbial growth and being completely overlooked [19]. As siderophore bountiful in nature, iron is not effortlessly production by fungi in marine habitats is an available to microbes due to formation of ferric interesting yet under explored area, this article oxyhydroxide at neutral to alkaline pH in which mainly focuses on siderophores produced by [2, 3] the earth abounds . To combat this stress marine-derived fungi. Our laboratory had microbes (mostly aerobic bacteria, fungi and contributed some pioneering work in this field. others) have developed a strategy i.e. chelation Vala et al. (2000) [20] had reported their work on through production of siderophores. siderophores of facultative marine fungi. They Siderophores are low molecular weight had worked with thirteen strains out of which, 3+ [4, compounds with the strongest affinity for Fe ten produced siderophores which were 5] 3+ 2+ . They facilitate the conversion of Fe to Fe recognized as hydroxamates and carboxylates. [6] and make it available to microbes . The term Rests of three strains were non siderophore ‘siderophore’ had been coined from Greek word producers. The absence of siderophores in meaning “iron bearer”. The first siderophore marine environment may be due to diffusion discovered was ferrichrome produced by which makes siderophore production an Ustilago sphaerogena which can work as unprofitable exercise for the isolates. Other [7] growth factor for others . Siderophores have reason could be replacement of ferredoxins by gained interest in medical science due to its iron flavodoxin which requires Mn2+ rather than Fe3+ chelating efficiency for example, in some marine isolates. However, imperative Deferrioxamine-B – a natural siderophore need for iron-dependent respiratory chains for produced by Streptomyces pilosus is broadly aerobic life cannot be overlooked hence, non- used in iron overload conditions during repeated detection could also be a possibility than non- [8] blood transfusions . While focusing on marine production [21-24]. In their study, carboxylates habitat, large ocean regions are known as high were reported in mucoraceous fungi as well as a nitrate low chlorophyll (HNLC) because of low non mucoraceous fungus Paecilomyces variotii. chlorophyll content in photosynthetic Others were found to produce hydroxamate microorganisms. This HNLC region contains siderophores. Baakza et al., 432 INDIAN J. MAR. SCI., VOL. 45, NO. 3 MARCH 2016 (2004)[24] had given comparative data on hydroxy-L-ornithine with different possible acyl siderophore production of marine and terrestrial groups. These units are covalently linked via fungi. They had selected ten marine and ten ester or peptide bonds to linear or cyclic terrestrial fungal isolates. Screening these fungal oligomeric iron chelators by nonribosomal isolates for siderophore production revealed peptide synthetases (NRPSs) in the third step valuable information about abundance of these and finally the NRPS products can be altered molecules in both the habitats. Amongst these, a further by non-NRPS enzymes in order to yield marine fungus Cunninghamella elegans was siderophore diversity [26, 28, 29]. found to produce maximum (1987.5 µg/mL) siderophores while terrestrial C. elegans produced 1248.75 µg/mL indicating that marine fungi are equally important source of siderophores though less exploited. Some marine-derived fungi proved to be even more efficient siderophore producers when compared with terrestrials. Vala et al., (2006)[25] had reported data regarding aspergilli from two different habitats: five from marine and five from terrestrial. Aspergillus versicolor, a marine isolate synthesized the highest 182.5 µg/mL on the fifteenth day and the lowest producers also were marine Aspergillus sp. and Aspergillus niger. Moreover, aspergilli from both the habitats were producers of hydroxamate siderophores. Looking to the importance of marine-derived fungal siderophores which are yet under explored, our laboratory has extended the work on their role in mangrove reclamation by [Fig. 1 Biosynthetic pathway of siderophores from A. examining thirty four fungal isolates associated fumigatus and A. nidulans (Adapted from Gründlinger et with mangrove Avicennia marina along Gujarat, al., (2013a) [30]] West Coast of India. Among these thirty four [30] fungal isolates, thirty two produced Blatzer et al., (2011) identified and 5 siderophores, again confirming wide distribution characterized sidL (encoding N - 5 of siderophore production potential among hydroxyornithine:acetyl coenzyme A (CoA)-N - mangrove associated fungi (Data unpublished). transacylase), the first siderophore biosynthetic gene not to be regulated by iron availability. Molecular mechanism of siderophore They reported that the sidL is not genomically biosynthesis and uptake clustered with other siderophore-biosynthetic genes. Siderophore biosynthesis in fungi Recently, Gründlinger et al., (2013a)[31] identified a new component (SidJ) of Genes involved in siderophore biosynthesis, siderophore metabolism in Aspergillus uptake and iron regulation in fungi have been fumigatus and reported its role in intracellular well documented by Haas (2003)[26] and Haas et siderophore hydrolysis. The gene encoding SidJ al., (2008)[27]. Elucidation of several unexplored was found to be localized in siderophore aspects has been pursued further by several biosynthesis gene cluster. Furhter, Gründlinger workers. While most fungal siderophores are [32] et al., (2013b) demonstrated partial hydroxamates, hydroxylation of L-ornithine by localization of fungal siderophore biosynthesis ornithine-N5-monooxygenase to N5-hydroxy-L- in peroxisome and reported the ornithine is the first step of the biosynthesis compartmentalization to be an evolutionary pathway (Fig.1). The hydroxamate group in the conserved region. Using green fluorescent second step is then formed by transferring an protein-tagging, the authors ascertained acyl group (from acyl-coenzymeA) to N5- peroxisomal localization of SidI (Mevalonyl- hydroxyornithine, resulting in N5 yl- N5 -ac - CoA TRIVEDI et al: MARINE-DERIVED FUNGAL SIDEROPHORES: A PERCEPTION 433 ligase), SidH (Mevalonyl-CoA hydratase) and outouterer membrane receptor proteins (OMRPs) in SidF (anhydromevalonyl-CCoAoA transferase) in A. both iron sufficient and deficient conditions by fumigatus. They suggested that as long as SidI, SDS-PAGE of rhizosphere associated fungi SidHSidH and SidF share the same compartment, from saline habitats viz. MucorMucor sp., Aspergillus efficient siderophore biosynthesis can be sp.1 and A. ambiguus. Results revealed 6-12 achieved in both peroxisome and the cytosol. prproteinsoteins expressed under iron limiting condition Johnson et al., (2013) [33] examined siderophore which couldcould be the surface receptors responsible biosynthesis in foliar grass endophytic fungus foforr siderophore promoted iron transport [40-42]. Epichloë festucae aandnd identified the role of sidN (e(encodingncoding siderophore synthetase) in Fungi generally take-up siderophore-iron biosynthesis of extracellular siderophore chechelateslates through transporters of unknown major epichloënin A which is related to ferrirubin of facilitator (UMF)/ siderophore iron transporter [27, 43, 44] the ferrichrome family. Yasmin et al., (2012) [34] (SIT) subfamily . The siderophore demonstrateddemonstrated a link between siderophore transporters are one of the seventeen protein triacetylfusarinine C (TAFC) and ergosterol fafamiliesmilies exclusively found in fungi. Most of the biosynthetic pathways. They identified sidI and information
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