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Marine-Derived Fungal Siderophores: a Perception

Marine-Derived Fungal Siderophores: a Perception

Indian Journal of Geo-Marine Science Vol. 45(3) March 2016, pp. 431-439

Marine-derived Fungal : 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 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 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 concentration affecting the primary production. Marine 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. 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 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 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 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 about siderophore-iron transporter sidH encoding acyl-CoA ligase and enoyl-CoA iinn fungi is from the yeast Saccharomyces hydratase, respectively, in A. fumigatus. Initially cerevisiae, which does not synthesize while working with cubense, Anke siderophores but can take-up xenosiderophores and Diekmann (1974)[35] proposed the role of using membrane siderophore-iron transporters [45] such enzymes in biosynthesis of fusarinine-type . A. fumigatus has been predicted to encode [46] siderophores. ten siderophore iron transporters . MirA, While much of the information on siderophore MiMirB,rB, and MirC have been identified as biosynthhesisesis is available for aspergilli, Lehner et siderophore transporters in A. nidulans, the al., (2013)[29] examined ten wild type strains of expexpressionression of which is regulated by the [45, 47-49] Trichoderma and found high degree of diversity transcription factors SreASreA and HapX . among siderophores. They suggested further modificationsmodifications of the MiMirBrB was hypothesized to mediate siderophore uptake in A. fumigatus by Haas et al., (2008) [27], synthetase (NRPS) products to be responsible [45] for the high diversity. They prproposedoposed that the later Raymond-Bouchard et al., (2012) fusarinine-ttypeype siderophore biosynthesis by pursued the siderophore-iron uptake by the Trichoderma iiss similar to well-understood transporter MirB from the same fungus in detail process in Aspergillus sp. and reported its ability to transport siderophores coprogen, ferricrocin and TAFC as well. Not only the genes involved in siderophore metabolism have been iidentifieddentified and characterized, but the supply of substrate for siderophore biosynthesis from different organelles has also been studied recently. Beckmann et al., (2013)[36] have reported the role of mitochondrial ornithine rather than cytosolic ornithine in siderophore biosynthesis in A. fumigatus.

Transport of iron-ssiderophoreiderophore complex in fungi

MicroorganismsMicroorganisms depend on receptors present in various compartments of the cell envelope for siderophore uptake. There are four different mechanisms for siderophororee mediated Fe3+ transport in fungi[37,38] as depicted in Fig. 2. Hajela (2010)[39] had studied the expression of [Fig. 2 Siderophore mediated iron transport in fungi]

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Though molecular details of siderophore Screening and Detection of siderophores metabolism in fungi is being given due ScrScreeningeening procedures for siderophore attention,attention, the case is all the more critical for production by terrestrial and marine isolates marine-derderivedived fungi. Several fungi from marine include Fecl test [55], Chrome Azurol S (CAS) environment have been observed to produce 3 assay and CAS agar plate test[56]. In case of siderophores [19, 20, 25, 50]. However, scant detection of siderophores from marine-derived information exists about molecular details of fufungi,ngi, we have observed [Fig. 3] that modified siderophores of this ggrouproup of fungi [51]. CAS agar[57] suitedsuited better. CAS agar plate Status of siderophore biosynthesis in marine- contains Hexadecyltrimethylammonium derived fungi (HDTMA), a detergent that is toxic to growth of the cells. Hence, siderophore production is [52] Wang et al., (2009) purified and identified the inhibited. In modified CAS agar plate, half of siderophore of a marine-derived yeast the plate contains CAS and half growth medium. Aureobasidium pullulans HN6.2 as fusigen As only half of the plate contains CAS, having strong antibacterial activity against HDTMA does not hinder the growth of the Vibrio anguillarum. They observed expression fungus. Thus, siderophores appears as orange- 5 of gene encoding ornithine N -oxygenase reredd zones around the fungal growth [Fig. 3]. (catalyzing(catalyzing first committed step in siderophore biosynthesis) at transcription level and reported that the gene was repressed and enhanced in presence of iron and orniithine,thine, respectively.

Recently, Chi et al., (2012)[51] cloned and characterized sidA gene (L-Ornithine-N5- [Fig. 3 Siderophore production on (a) CAS agar plate and (b) Modified CAS agargar plate by marine-derived isolate] MonooxygenaseMonooxygenase structural gene) from a marine- derived yeast A. pullulans HN6.2 and Chemical Nature of Siderophores established physiological role of siderophore in SiSiderophoresderophores are chemically categorized marine-derived yeaeasts.sts. The cloned gene was according to the functional group used to co- found to be 1461 bp encoding 486 amino acid ordinate Fe3+. Siderophores are mainly protein with molecular weight 55.4kDa. The characterized as hydroxamates, catecholates, authors observed a negative effect of deleting 5 carboxylates, mixed type siderophores and a the gene encoding L-ornithine-N - suite of amphiphilic siderophores (produced monooxygenasemonooxygenase on asexual reproduction of the exclusively by marine bacteria). Chemical test organism. [53] nature of siderophores can be detected by Further, Chi et al., (2013) isolated and chemical as well asas bioassays. Bioassays are characterized the SRE1 (GATA Type more sensitive than chemical assays which transcription repressor) and studied the effect of include the use of transport defective indicator gene disruption on biosynthesis of siderophores strains. and expression of sidA ggene.ene. The expression of HydroxamateHydroxamate siderophores are known to be sidA gene was greatly de-repressed at produced by bacteria and by most fungi [58, 59]. transcriptiontranscription level when the disruptant (R6) was HyHydroxamatedroxamate nature of siderophore is confirmed grown in iron-rerepletedpleted medium. The authors are [60] by FeCl3 test showing λmax between 420-450 still exploring how does the Sre1 bind to the nm and tetrazolium salt test[61]. Bioassay for promoter of sidA gene, as the promoter for sidA hyhydroxamatedroxamate is carried out by using contains the sequence 5’-HGATAR-3’ and not [62] [51] Arthrobacter flavescens JG9 . Marine the sequence 5’-ATCWGATAA-3’ . Haas et aspergilli like, Aspergillus sp., A. versicolor and al., (1999)[54] reported derepression of L- 5 A. niger are also known to produce hydroxamate ornithine-N -oxygenase activity and siderophores [25]. Wang et al., (2009)[52] have consequently derepression of the biosynthesis of reported marine-derived A. pullulans to produce the hydroxamate siderophore N,N’,N’- siderophore fusigen, a type of hydroxamate triacetylfusarinine in A. nidulans when supplied siderophore (Fig. 4). with sufficient iron concentration.

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sisiderophores.derophores. Further structural characterization of this siderophore is in progress in our laboratory. Amphiphilic siderophoresderophores have one or two series of fatty acid attached with head group which co ordinates with Fe3+. Amphiphilic [Fig. 4 FFusigenusigen siderophore from marine-derived [52] sisiderophorederophore like amphibactins (Vibrio sp.18) Aureobasidium pullulans ] and ochrobactins (Ochrobactrum sp.18) are Hydroxamate siderophores are further hyhydrophobicdrophobic in nature while loihichelins categorized as mono-, di- and tri-hydroxamates, (Halomonas sp.LOB5) are hydrophilic. basedbased on number of hydroxamate groups. Based Amphiphilicity is based on variations in on the number of bonds the forms with composition of head group relative to fatty acid metal ion, ligand denticity identifies them as bi-, chain length. To the best of our knowledge so tetra- and hexadentates. Vala et al., (2006)[25] far amphiphilic siderophores have not been observedobserved occurrence of trihydroxamate reported in marine-derivedderived fungi. hexadentate siderophores in marine as well as It was normally believed that all fungal terrestrial aspergilli. A higher stability constant siderophores were hydroxamates but then of hexadentates is the reason behind their Winkelmann (1991)[66] proposed a new predominance over bi- and tetradentates [63] in siderophore from Rhizopus microsporus bothboth marine and terrestrial environment. In our shoshowingwing the presence of citric acid and named it recent study, out of thirty two isolates, thirty one rhizoferrin. Carboxylates are exclusively belonging to Ascomycota pproducedroduced hydroxamate produced by fungi belonging to Mucorales and a siderophores as expected. Among these thirty few bacteria [67]. They are detected by one isolates, twenty seven produced spectrophotometric analysis [68] and bioassay trihydroxamate hexadenexadentatestates whereas four using Morganella morganii [62]. One of the produced tetradentates which is a novel strains of marine-derived P. variotii also behavior. prproducedoduced carboxylate siderophore and hence CatCatecholateecholate nature of siderophore can be exhibited occurrence of carboxylate outside [60] [20] detected by FeCl3 test shoshowingwing λmax at 495 Mucorales . The siderophore produced by C. nm, Arnow’s test[64] and bioassay by using elegans ATCC36112 was identified and Salmonella typhimurium enb-7[62]. Catecholate confirmed as rhizoferrin by using one and two siderophores having as functional dimensional NMR [19]. The authors [19] compared group were initially reported to be produced tthehe observed data with published data[69,70] for only by bacteria. One of the marine fungal the identification and confirmation of strains of Penicillium bilaii exexhibitedhibited a novel rhizoferrin. A possible role of marine fungal behavior. This strain produced pistillarin siderophores in hydrocarbon degradation, a siderophore which is chemchemicallyically a catecholate pollutant extensively contaminating marine when grown under relatively high iron environment is under process in our laboratory. [65] concentrations . The structure of pistillarin is MiMixedxed types of siderophores show great as shown in (Fig. 5). diversity of structures as in fluorescent psepseudomonadsudomonads that produce exemplified by extracelluar production of yellow-greengreen fluorescent pigment [71]. StStructuresructures of only few of the siderophores from [65] [Fig. 5 Pistillarin siderophore from Penicillium bilaii ] marine-derivedderived fungal isolates have been characterized and analyzed. Further In our recent study (data unpublished) one of the investigations in this line could be an interesting strains yet to be identified has also shown area of research. production of catecholate and hydroxamate

Applications SiderophoreSiderophore production is not restricted to

laboratory conditions but also found in and aquatic conditions. Hence, they have significant

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ecological as well as economical roles. Some of [83]. While some of the them are described below. conventional methods used prove unsuitable economically and also result in degradation of Selective utilization of siderophores in mixed soil texture [84], application of siderophores for microbial populations is a key mechanism for bioremediation of metal contamination could be preventing emergence of unwanted competing a promising alternative. In metal contaminated organisms. soil that is iron deficient, microorganisms There are various applications of siderophores producing siderophores reduce the metal load as reported in medical field. When siderophores they can chelate other metals like nickel also bind with , they form sideromycins, a besides iron. new way for drug delivery. Artemisinin, an anti- Siderophores are known to play a significant malarial agent combines with analogue of role in cellulose depolymerization and lignin Mycobactin expressing antituberculosis activity modification. It may be possible to function with in M. tuberculosis [72]. Siderophore produced by Mn as the catalyst for depolymerization process Klebsiella pneumoniae had been used as anti- which could open the wood structure to allow malarial agent [73], and also as deodorants [74]. penetration of large enzyme because of low Deferrioxamine well known for its use in iron molecular weight of siderophore-metal overload conditions has also been used in complexes and oxidizing potential of the removal of [75]. The medical transition metals. Siderophores are known to applications of siderophores of marine origin are scavenge transition metals for extracellular yet to be explored. enzyme production and fungal metabolism [85]. Siderophores also play an important role in It has been reported recently [86] that dissolution agriculture. putida produces of spent nuclear fuel is influenced even by low pseudobactin which enhances plant growth concentration of siderophores, be it synthetic when soil is inoculated with these organisms [76]. desferrioxamine or pyoverdines synthesized by Systemic resistance is thought to be induced by . Siderophores are siderophores in plants causing disease proposed to play a role in radioactive waste suppression [77]. Siderophores produced by remediation and nuclear fuel reprocessing [38]. bacteria with higher chelating efficiency makes iron availability restricted for pathogens and lets Exceptional Fe3+ binding constant of the bacteria succeed in competition [78, 79]. Study siderophores make them an ideal selection for on role of siderophores of marine-derived fungi molecular recognition element and they could be in biocontrol of plant pathogens is in progress in used for detecting Fe-bioavailability in or our laboratory. oceanic water [87]. Pesce and Kaplan 1990[88] had proposed pyoverdines as suitable candidates for produced by fluorescent construction of biosensor. pseudomonads could be an important tool to diversify closely related strains[80, 81]. Strains Acknowledgements having identical pyoverdine show same iso electrical focusing (IEF). On other hand Thanks are due to the Department of Science different pyoverdines exhibit different IEF and Technology, Government of India, New patterns. Based on the patterns exhibited by Delhi, for sanctioning financial support under siderophores in IEF, siderotyping involves Women Scientists Scheme [SR/WOS-A/LS- separation of siderophores based on their iso 307/2013(G)] to AKV. electric pH. References 1. Guan, L.L., Kanoh, K., Kamino, K., Effect of Marinobacter hydrocarbonoclasticus, an oil exogenous siderophores on iron uptake activity degrading marine bacterium isolated by Barbeau of marine bacteria under iron limited conditions, et al., (2003) [82] have been reported to produce Appl. Environ. Microbiol., 67(2001) 1710-1717 petrobactin. It has been suggested that 2. Crosa, J.H., Genetics and molecular biology of siderophore-mediated iron transport in bacteria hydrocarbons can be degraded by iron Microbiol. Rev., 53(4) (1989) 517–530 facilitation in bacteria present in marine 3. Neilands, J.B., Iron absorption and transport in ecosystems. microorganisms. Annu. Rev. Nutr., 1(1981) 27-46 4. Lankford, C.L. Bacterial assimilation of iron, Soil contaminated with heavy metals is a major Crit. Rev. Microbiol., 2(1973) 273-331 problem that warrants attention for TRIVEDI et al: MARINE-DERIVED FUNGAL SIDEROPHORES: A PERCEPTION 437

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