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Labrenzbactin from a Coral-Associated Bacterium Labrenzia Sp

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Labrenzbactin from a Coral-Associated Bacterium Labrenzia Sp View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Diponegoro University Institutional Repository The Journal of Antibiotics https://doi.org/10.1038/s41429-019-0192-x BRIEF COMMUNICATION Labrenzbactin from a coral-associated bacterium Labrenzia sp. 1 1 1 1 2 1 Amit Raj Sharma ● Tao Zhou ● Enjuro Harunari ● Naoya Oku ● Agus Trianto ● Yasuhiro Igarashi Received: 14 February 2019 / Revised: 7 April 2019 / Accepted: 16 April 2019 © The Author(s), under exclusive licence to the Japan Antibiotics Research Association 2019 Abstract A new catecholate-containing siderophore, labrenzbactin (1), was isolated from the fermentation broth of a coral-associated bacterium Labrenzia sp. The structure and absolute configuration of 1 was determined by spectroscopic methods and Marfey’s analysis. Overall, 1 showed antimicrobial activity against Ralstonia solanacearum SUPP1541 and Micrococcus luteus ATCC9341 with MIC values of 25 and 50 µg ml−1, respectively, and cytotoxicity against P388 murine leukemia cells with an IC50 of 13 µM. Marine microorganisms are attracting much attention as a polyketide-derived pederin analog and two cyclopropane- source of new compounds alternative to terrestrial micro- containing fatty acids have been reported [8, 9]. 1234567890();,: 1234567890();,: organisms [1]. The number of new compounds from marine In our investigation of secondary metabolite production microorganisms is steadily increasing in recent years [1, 2]. by coral-associated bacteria, Labrenzia sp. C1-1 was found A large portion of marine microorganisms are likely asso- to produce a new catecholate-class siderophore designated ciated with host organisms, especially marine invertebrates, labrenzbactin (1, Fig. 1). In this paper, we describe the colonizing outside and/or inside of the host body and isolation, characterization, and bioactivity of 1. forming microbial communities unique to each host species The producing strain C1-1 was isolated from a cultured [3]. Such host-associated microorganisms are suggested to Scleractinian (stony) coral Montipora sp., and identified as a have a beneficial role in protecting the host from invading member of the genus Labrenzia by 16S rRNA gene or opportunistic pathogens, presumably by producing anti- sequence analysis. The whole culture broth of strain C1-1 microbial substances [4]. cultured in A3M seawater medium was extracted with 1- Labrenzia species are Gram-negative, aerobic, motile, butanol. After evaporation, the extract was fractionated by a and rod-shaped bacteria of the class Alphaproteobacteria. sequence of chromatographies, and the final purification They require NaCl for growth and are isolated from marine was achieved by reversed-phase HPLC to give lab- habitats, in many reported cases, in association with marine renzbactin (1). invertebrates such as corals [5–7]. Although the species of Compound 1 was obtained as a brown amorphous solid. Labrenzia possess biosynthetic genes for the production of The molecular formula of C32H36N4O10 with 17 degree of polyketide, non-ribosomal peptide, and terpenoid [7], very little is known about their secondary metabolites. To date, a Supplementary information The online version of this article (https:// doi.org/10.1038/s41429-019-0192-x) contains supplementary material, which is available to authorized users. * Yasuhiro Igarashi [email protected] 1 Biotechnology Research Center and Department of Biotechnology, Toyama Prefectural University, 5180 Kurokawa, Imizu, Toyama 939-0398, Japan 2 Faculty of Fisheries and Marine Sciences, Diponegoro University, Tembalang Campus, St. Prof. Soedarto, SH Semarang 50275 1 Central Java, Indonesia Fig. 1 Structure of labrenzbactin ( ) A. Raj Sharma et al. unsaturation was determined by HRESITOFMS that gave a dinitrophenyl-5-D-leucinamide (D-FDLA) using LC–MS. molecular ion [M + Na]+ at m/z 659.2324 (calcd for The derivatized L-serine standard with L-FDLA and C32H36N4O10Na, 659.2329) and NMR spectroscopic data D-FDLA eluted at 9.5 and 10.7 min, respectively, while the (Table 1). The IR spectrum of 1 indicated the presence of L-FDLA derivative of the acid hydrolysate of 1 eluted at OH and/or NH (3313 cm−1) and carbonyl (1634 cm−1) 9.5 min. The serine residue was determined to have the L- groups. Our in-house UV database indicated that the UV configuration and thus the configuration of C2 was estab- spectrum with the absorption bands at λmax 208, 250, and lished to be S (Fig. 1). 314 nm was similar to those for catechoserine (211, 248, Biological activity of labrenzbactin (1) was evaluated by and 319 nm) [10] or ulbactin F (204, 252, and 317 nm) [11], cytotoxicity and antimicrobial assays. Overall, 1 showed suggestive of the presence of a hydroxylated benzene ring moderate cytotoxicity against P388 murine leukemia cells at conjugated with a double bond like a carbonyl group. IC50 13 μM(IC50 of a reference drug doxorubicin: 0.018 μM) NMR spectroscopic data of 1 revealed the presence of 32 and no appreciable activity in antimicrobial assay against carbons attributable to four carbonyl-like deshielded sp2 Bacillus subtilis ATCC6633, Staphylococcus aureus carbons, eighteen sp2 carbons (nine are proton-bearing), FDA209P JC-1, Rhizobium radiobacter NBRC14554, and eight methylenes, one methine, and one methoxy group Escherichia coli NIHJ JC-2. However, it showed weak (Table 1). COSY analysis identified proton resonances for antibacterial activity against Ralstonia solanacearum three sets of 1,2,3-trisubstituted benzene rings, H8/H9/H10, SUPP1541 and Micrococcus luteus ATCC9341 with MIC H9′/H10′/H11′, and H8″/H9″/H10″ (Fig. 2). HMBC cor- values of 25 and 50 µg ml−1,respectively. relations from H8 and H10 to C6 and H9 to C5 and C7 In summary, our chemical investigation of a marine established the 2,3-dihydroxyphenyl substructure. An oxa- bacterium Labrenzia led to the discovery of labrenzbactin zoline ring was deduced from the HMBC correlations from (1). It is a new member of bacterial siderophores in which a H2 and H3 to C4 and chemical shift consideration for H2, linear triamine, spermidine or norspermidine, is amidated H3, and C4. The linkage between C4 and C5 and the with acyl groups containing 2,3-dihydroxyphenyl and/or 2- attachment of C1 to C2 were determined by the observed hydroxyphenyl units (Fig. 3). Several related compounds HMBC correlations. Another 2,3-dihydroxyphenyl moiety are reported: parabactin (2)[13] from Paracoccus deni- consisting of the carbons from C5″ to C10″ and a 2- trificans; agrobactin (3)[14] from a plant pathogen Agro- hydroxy-3-methoxyphenyl moiety comprising C6′ to C11′ bacterium tumefaciens (currently Rhizobium radiobacter); were also established by analyzing HMBC correlation data. fluvibactin (4)[15], and vibriobactin (5)[16] from Vibrio The position of the methoxy group was confirmed by NOE fluvialis and Vibrio cholerae, respectively. detected between H12′ and H9′. The COSY spectrum also provided two short methylene chains from H1′ to H4′ and from H1″ to H3″. Mutual HMBC correlations between H1′ Experimental section and H1″ linked these carbon chains through a nitrogen atom, which was in turn connected with the carbonyl carbon General experimental procedure C1 by HMBC correlations from H1′ and H1″ to C1. Finally, two aromatic parts were connected to the methylene chains Optical rotation was measured using a JASCO DIP-3000 via an amide bond, on the basis of HMBC correlations from polarimeter. The UV spectra were recorded on a Shimadzu H4′ and H11′ to C5′ and from H3″ and H10″ to C4″ to UV-1800 spectrophotometer. The IR spectrum was mea- complete the planar structure of 1 (Fig. 2). This structure sured on a PerkinElmer Spectrum. NMR spectra were was further validated by analyzing the NMR spectral data obtained on a Bruker AVANCE 500 spectrometer in a obtained in DMSO-d6 that gave a higher peak resolution for mixture of CDCl3 and CD3OH (9:1) due to the low solu- 1 H NMR spectrum (Supplementary Information). Some of bility of 1 in a single solvent or in DMSO-d6. The residual 1 13 the H and C NMR signals were observed as duplicated solvent signals (CDCl3: δH 7.26 and δC 77.24; DMSO-d6: δH peaks, presumably due to the tautomeric isomerization of 2.50 and δC 39.5) were used as internal standards. HRE- amide bonds, but all the signals could be assigned to its SITOFMS was recorded on a Bruker micrOTOF focus mass structure (Table 1). The absolute configuration of the oxa- spectrometer. zoline moiety derived from serine in 1 was determined by the advanced Marfey’s analysis [12]. Following acid- Microorganism catalyzed hydrolysis, 1 was derivatized using 1-fluoro-2,4- dinitrophenyl-5-L-leucinamide (L-FDLA) and retention Strain C1-1 was isolated from a cultured stony coral time was compared with L-serine standard that was simi- (Montipora sp.) purchased from an aquarium vendor in larly derivatized with L-FDLA and 1-fluoro-2,4- Nagasaki, Japan. The coral specimen was washed with 70% Labrenzbactin from a coral-associated bacterium Labrenzia sp. 1 13 Table 1 H and C NMR data for labrenzbactin (1) in CDCl3–CD3OH (9:1) and in DMSO-d6 CDCl3–CD3OH (9:1) DMSO-d6 a b b,c a b Position δC δH mult (J in Hz) HMBC δC δH mult (J in Hz) 1 169.8, C 168.5/168.6 2 65.4, CH 5.16 t (8.4) 1, 3, 4 64.3 5.36 t (8.5)/5.37 t (8.5) 3 69.0, CH2 4.48 t (8.9) 1, 2, 4 69.3 4.53 t (9.0) 5.08 t (7.5) 1, 2, 4 4.76 t (7.3) 4 167.4, C 166.0 5 110.2, C 110.1 6 147.5, C 148.1 7 145.0, C 145.7 8 119.1, CH 6.99 d (7.2) 6, 10 119.5 6.96 d (7.6) 9 119.3, CH 6.75 t (7.3) 5, 7 118.8 6.74 t (8.0) 10 119.4, CH 7.15 d (7.9) 4, 6,
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