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MDN-0170, a New Napyradiomycin from Streptomyces Sp. Strain CA-271078

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MDN-0170, a New Napyradiomycin from Streptomyces Sp. Strain CA-271078 marine drugs Article MDN-0170, a New Napyradiomycin from Streptomyces sp. Strain CA-271078 Rodney Lacret *, Ignacio Pérez-Victoria, Daniel Oves-Costales, Mercedes de la Cruz, Elizabeth Domingo, Jesús Martín, Caridad Díaz, Francisca Vicente, Olga Genilloud and Fernando Reyes * Fundación MEDINA, Centro de Excelencia en Investigación de Medicamentos Innovadores en Andalucía, Avda. del Conocimiento 34, 18016 Armilla (Granada), Spain; [email protected] (I.P.-V.); [email protected] (D.O.-C.); [email protected] (M.d.l.C.); [email protected] (E.D.); [email protected] (J.M.); [email protected] (C.D.); [email protected] (F.V.); [email protected] (O.G.) * Correspondence: [email protected] (R.L.); [email protected] (F.R.); Tel.: +34-958-993-965 (F.R.) Academic Editor: Miguel O. Mitchell Received: 11 August 2016; Accepted: 13 October 2016; Published: 18 October 2016 Abstract: A new napyradiomycin, MDN-0170 (1), was isolated from the culture broth of the marine-derived actinomycete strain CA-271078, together with three known related compounds identified as 4-dehydro-4a-dechloronapyradiomycin A1 (2), napyradiomycin A1 (3) and 3-chloro- 6,8-dihydroxy-8-α-lapachone (4). The structure of the new compound was determined using a combination of spectroscopic techniques, including 1D and 2D NMR and electrospray-time of flight mass spectrometry (ESI-TOF MS). The relative configuration of compound 1, which contains two independent stereoclusters, has been established by molecular modelling in combination with nOe and coupling constant analyses. Biosynthetic arguments also allowed us to propose its absolute stereochemistry. The antimicrobial properties of the compounds isolated were evaluated against methicillin-resistant Staphylococcus aureus (MRSA), Escherichia coli, Aspergillus fumigatus, and Candida albicans. The potent bioactivity previously reported for compounds 2 and 3 against methicillin-sensitive S. aureus has been extended to methicillin-resistant strains in this report. Keywords: Streptomyces; napyradiomycin; structural elucidation; antimicrobial activity 1. Introduction The napyradiomycins (NPDs) constitute an interesting family of halogenated natural compounds mainly produced by bacteria of the family Streptomycetaceae, which were first discovered from cultures of the actinomycete Chainia rubra [1,2], later reclassified as Streptomyces ruber [3]. This class of secondary metabolites consists of a naphthoquinone core, a prenyl unit attached at C-4a, a monoterpenoid substituent at C-10a, and some congeners have a methyl group at C-7 [1,4–6]. At present, nearly 47 different NPDs have been described [1,2,4–12]. Compounds belonging to this structural class possess significant antibacterial activity against pathogenic bacterial strains such as methicillin-resistant Staphylococcus aureus (MRSA) and inhibit the growth of several tumor cell lines [13–15]. In the course of our continuous search for new bioactive natural products from marine actinomycetes, over 400 marine-derived strains were grown in carefully selected media and their fermentations extracts were assayed against clinically relevant pathogenic microbial strains [16]. Growth inhibition of MRSA was observed in the acetone crude extract from fermentation broths of strain CA-271078, which upon 16S rRNA sequencing was found to be closely related to Streptomyces aculeolatus NBRC 14824(T). A bioassay-guided fractionation of the ethyl acetate extract of this microorganism and a dereplication by LC/MS of the bioactive fractions was carried out in order Mar. Drugs 2016, 14, 188; doi:10.3390/md14100188 www.mdpi.com/journal/marinedrugs Mar.Mar. Drugs Drugs2016 2016, 14, 14, 188, 188 2 of2 of 12 12 this microorganism and a dereplication by LC/MS of the bioactive fractions was carried out in order toto isolate isolate and and identify identify the the new new chemicalchemical constituents that that were were responsible responsible for for the the activities activities observed. observed. HereinHerein we we report report the the isolation isolation of MDN-0170of MDN‐0170 (1), a(1 new), a new napyradiomycin napyradiomycin alongside alongside three relatedthree related known compoundsknown compounds (2–4). The ( structural2–4). The elucidationstructural elucidation of MDN-0170 of wasMDN accomplished‐0170 was accomplished using a combination using a of spectroscopiccombination of techniques, spectroscopic including techniques, HRMS including and extensive HRMS and 1D andextensive 2D NMR 1D and analyses 2D NMR in combination analyses in withcombination molecular with modelling. molecular modelling. 2.2. Results Results andand DiscussionDiscussion 2.1.2.1. Isolation Isolation and and Taxonomy Taxonomy of of the the Producing Producing Microorganism Microorganism TheThe producing producing strain, strain, CA-271078, CA‐271078, was was isolatedisolated from an ascidian collected collected at at the the sea sea shore shore in in Baía Baía AnaAna Chaves, Chaves, Sao Sao Tome Tome (Sao (Sao Tome Tome and and Principe). Principe). A BLASTNA BLASTN search search employing employing the the PCR-amplified PCR‐amplified 16S rRNA16S rRNA sequence sequence (1359 bp)(1359 indicated bp) indicated that the that strain the wasstrain related was related to Streptomyces to Streptomyces aculeolatus aculeolatusNBRC 14824(T)NBRC (99.34%14824(T) similarity) (99.34% similarity) [17]. A phylogenetic [17]. A phylogenetic tree was tree constructed was constructed using the using neighbor-joining the neighbor‐joining method correctedmethod corrected with the with Jukes-Cantor the Jukes‐Cantor algorithm algorithm [18,19 [18,19]] (Figure (Figure1) showing1) showing the the relatedness relatedness with StreptomycesStreptomyces aculeolatus aculeolatusNBRC NBRC 14824(T) 14824(T) (99.34% (99.34% similarity)similarity) and Streptomyces synnematoformans synnematoformans S155(T)S155(T) (98.73%(98.73% similarity). similarity). TheThe remainingremaining closestclosest members of of the the genus genus StreptomycesStreptomyces exhibitedexhibited sequence sequence similaritiessimilarities below below 98%. These These data data strongly strongly indicate indicate that thatstrain strain CA‐271078 CA-271078 is a member is a member of the genus of the genusStreptomycesStreptomyces. S. javensis NBRC 100777T (AB249940) 69 S. violaceusniger NBRC 13459T (AB184420) 81 S. yogyakartensis NBRC 100779T (AB249942) S. albiflaviniger NRRL B-1356T (AJ391812) 60 S. demainii NRRL B-1478T (DQ334782) S. hygroscopicus NRRL 2387T (AB231803) 94 S. endus NRRL 2339T (AY999911) S. sporocinereus NBRC 100766T (AB249933) S. castelarensis DSM 40830T (AY508511) 68 S. mordarskii NRRL B-1346T (EF408735) 53 96 S. melanosporofaciens NBRC 13061T (AB184283) S. antimycoticus NBRC 12839T (AB184185) 64 S. sporoclivatus NBRC 100767T (AB249934) 62 S. rapamycinicus NRRL 5491T (EF408733) S. morookaense LMG 20074T (AJ781349) 98 S. lacticiproducens GIMN4.001T (GQ184344) S. albospinus NBRC 13846T (AB184527) 66 63 S. angustmyceticus NBRC 3934T (AB184817) 80 S. ramulosus NRRL B-2714T (DQ026662) 69 S. caniferus NBRC 15389T (AB184640) S. cacaoi NBRC 12748T (AB184115) S. ruber NBRC 14600T (AB184604) S. synnematoformans S155T (EF121313) 99 Streptomyces sp. strain CA-271078 55 S. aculeolatus NBRC 14824T (AB184624) Micromonospora auratinigra TT1-11T (AB159779) 0.01 FigureFigure 1. 1. NeighborNeighbor-joining‐joining (NJ) (NJ) tree built tree with built MEGA with MEGA6.06 based 6.06 on nearly based‐complete on nearly-complete 16S rRNA gene 16S rRNAsequences gene of sequences CA‐271078 of and CA-271078 the closest and type the strains closest of typethe genus strains Streptomyces of the genus. MicromonosporaStreptomyces . Micromonosporaauratinigra TT1 auratinigra‐11(T) wasTT1-11(T) employed was as employedout‐group. asThe out-group. numbers The at the numbers nodes at indicate the nodes bootstrap indicate bootstrapsupport (%) support based (%) on basedNJ analysis on NJ of analysis 1000 replicates; of 1000 replicates;only values only higher values that higher 50% are that shown. 50% areThe shown. scale Thebar scale indicates bar indicates 0.01 substitutions 0.01 substitutions per site. per site. Mar. Drugs 2016, 14, 188 3 of 12 Mar. Drugs 2016, 14, 188 3 of 12 2.2. Extraction, Dereplication and Bioassay-GuidedBioassay‐Guided Isolation The producing strain CA CA-271078‐271078 was fermented at at 28 28 °C◦C in in 1 1 L L of of R358 medium for for six six days. days. Extraction withwith an an equal equal volume volume of acetoneof acetone and and evaporation evaporation of the of organic the organic solvent solvent afforded afforded an acetone an crudeacetone extract, crude whichextract, was which subsequently was subsequently subjected subjected to liquid-liquid to liquid extraction‐liquid extraction with ethyl with acetate ethyl (EtOAc). acetate This(EtOAc). organic This extract organic showed extract showed antibacterial antibacterial activity activity against against MRSA. MRSA. LC-UV-MS LC‐UV analysis‐MS analysis of the of ethyl the acetateethyl acetate extract extract revealed revealed the presencethe presence of some of some compounds compounds that that were were not not included included in in our our in-housein‐house microbial natural products library [20] [20] nor in the the Chapman & Hall dictionary of of Natural Natural Products Products [21]. [21]. The ethyl ethyl acetate acetate extract extract was was chromatographed chromatographed on
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