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Bioactive Molecules from Mangrove Streptomyces Qinglanensis 172205

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Bioactive Molecules from Mangrove Streptomyces Qinglanensis 172205 marine drugs Article Bioactive Molecules from Mangrove Streptomyces qinglanensis 172205 Dongbo Xu 1, Erli Tian 1, Fandong Kong 2 and Kui Hong 1,* 1 Key Laboratory of Combinatorial Biosynthesis and Drug Discovery, Ministry of Education, School of Pharmaceutical Sciences, Wuhan University, Wuhan 430071, China; [email protected] (D.X.); [email protected] (E.T.) 2 Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultura Sciences, Haikou 571101, China; [email protected] * Correspondence: [email protected]; Tel.: +86-27-6875-2442 Received: 17 April 2020; Accepted: 12 May 2020; Published: 13 May 2020 Abstract: Five new compounds 15R-17,18-dehydroxantholipin (1), (3E,5E,7E)-3-methyldeca-3,5,7- triene-2,9-dione (2) and qinlactone A–C (3–5) were identified from mangrove Streptomyces qinglanensis 172205 with “genetic dereplication,” which deleted the highly expressed secondary metabolite-enterocin biosynthetic gene cluster. The chemical structures were established by spectroscopic methods, and the absolute configurations were determined by electronic circular dichroism (ECD). Compound 1 exhibited strong anti-microbial and antiproliferative bioactivities, while compounds 2–4 showed weak antiproliferative activities. Keywords: mangrove Streptomyces; genetic dereplication; anti-microbial; antiproliferative 1. Introduction Microbial natural products are an important source of drug lead. Mangrove streptomycetes were reported as a potential source of plenty of antiproliferative or anti-microbial chemicals with novel structures [1]. The bioinformatics of easily available genome information from microorganisms breaks the bottleneck of traditional natural product discovery to a certain extent, and secondary metabolites isolation guided by genome sequence has increasingly become a research frontier [2]. Genome mining and silent gene cluster activation unveil the potential of diverse secondary metabolites in bacteria [3–5]. The OSMAC (One Strain Many Compounds) approach has been proven to be a simple and powerful tool to mine new natural products [6,7]. Due to complexity profiles of secondary metabolites including intermediates, a strategy named “genetic dereplication” was also developed to simplify the profiles by eliminating the major known secondary metabolites’ biosynthetic pathway, so that more easily detecting other novel compounds and/or reversing the precursor pools for other low expressed pathways in the microorganisms [8]. Previous studies reported that enterocin and its metabolites are the main and high-yield products in Streptomyces qinglanensis 172205 [9]. After the whole genome sequence was obtained, we analyzed the gene clusters of secondary metabolites, and found that more than 50% of them are coding for unknown compounds. However, enterocin was always detected in all of the media used during the OSMAC study. Hence, in this study, to mine the unknown compounds in strain 172205, we carried out the genetic dereplication strategy by which we deleted the enterocin biosynthetic gene cluster in genome and then detected the diversity of secondary metabolites profiles by OSMAC method. A mutant strain 172205Denc was generated by the whole enterocin biosynthetic gene cluster deletion using double-crossover homologous recombination and tested by HPLC fingerprint profiles for diverse products of crude extracts from 10 kinds of liquid fermentation media. The results showed Mar. Drugs 2020, 18, 255; doi:10.3390/md18050255 www.mdpi.com/journal/marinedrugs Mar. Drugs 2020, 18, 255 2 of 11 Mar. Drugs 2020, 18, x 2 of 11 that(dextrin strain-oatmeal) 172205D encmedium.could produceSubsequently, the most a diverselarge-scale peaks fermentation on HPLC under with fermentationD.O. medium in D.O.was (dextrin-oatmeal)performed. After medium. isolation Subsequently, and purification a large-scale of the fermentationcompounds withfrom D.O. the mediumcrude extract, was performed. five new Aftercompounds isolation including and purification 15R-17,18 of the-dehydroxantholipin compounds from the ( crude1), (3E extract,,5E,7E) five-3-methyldeca new compounds-3,5,7- includingtriene-2,9- 15dioneR-17,18-dehydroxantholipinMar. (2 )Drugs and 20 20qinlactone, 18, x A–C (1 ),(3 (3–E5),5 Ewere,7E)-3-methyldeca-3,5,7-triene-2,9-dione identified. Their structures were elucidated (2) and qinlactone2 of 11by one- A–Cdimensional (3–5) were (1D identified.)/two-dimensional Their structures (2D) nuclear were elucidated magnetic by resonance one-dimensional spectroscopy (1D)/two-dimensional (NMR) data, as (2D)well nuclear as(dextrin electronic magnetic-oatmeal) circular medium. resonance dichroism Subsequently, spectroscopy (ECD) calculation. a (NMR)large-scale data, In fermentationanti as-microbial well as electronicwith bioassay D.O. circularmedium tests, compound dichroismwas 1 (ECD)showedperformed calculation. strong. antiAfter In-Staphylococcus anti-microbialisolation and purifi aureus bioassaycation and tests,of anti the- compoundCandidacompounds albicans 1fromshowed theactivi crude strongties extract,with anti- MIC Staphylococcusfive (minimumnew aureusinhibitorycompoundsand anti-concentration)Candida including albicans 15valuesR-17,18activities of-dehydroxantholipin 0.78 withµg/ml MIC and (minimum 3.13(1), (3µg/ml,E,5E,7 inhibitoryE respectively.)-3-methyldeca concentration) -For3,5,7 antiproliferative-triene- values2,9- of dione (2) and qinlactone A–C (3–5) were identified. Their structures were elucidated by one- 0.78bioactivity,µg/mL andcompound 3.13 µg 1/mL, exhibited respectively. strong cytotoxicities For antiproliferative against human bioactivity, breast compound cancer cell1 lineexhibited MCF-7 dimensional (1D)/two-dimensional (2D) nuclear magnetic resonance spectroscopy (NMR) data, as strongand humanwell cytotoxicities as cervicalelectronic againstcancer circular cell human dichroism line He breast (ECD)La with cancer calculation. IC50 cell values line In anti MCF-7of 5.78-microbial µ andM and human bioassay 6.25 cervicalµ tests,M, respectively, compound cancer cell 1 while line HeLacompound withshowed IC 2 –50strong4 valuesshowed anti of-Staphylococcus weaker 5.78 µM antiproliferative and aureus 6.25 andµM, anti respectively, activit-Candidaies albicanswith while IC activi50 compound valuesties with ranging 2MIC–4 showed (minimumfrom 12 weaker9 to 207 antiproliferativeµM. Therefore,inhibitory concentration) the activities “genetic with dereplication”values IC 50of values0.78 µg/ml strategy ranging and is3.13 from useful µg/ml, 129 to torespectively.find 207 compoundsµM. For Therefore, antiproliferative that synthesized the “genetic by dereplication”low expressionbioactivity, strategy genecompound clusters is useful 1 exhibited and to would find strong compounds be cytotoxicities of interest that toagainst synthesized colleagues human inbybreast natural low cancer expression product cell line genediscovery. MCF clusters-7 and wouldand human be of cervical interest cancer to colleagues cell line He inL naturala with IC product50 values of discovery. 5.78 µM and 6.25 µM, respectively, while 2. Resultscompound 2–4 showed weaker antiproliferative activities with IC50 values ranging from 129 to 207 2. ResultsµM. Therefore, the “genetic dereplication” strategy is useful to find compounds that synthesized by Strainlow expression 172205Δ geneenc wasclusters obtained and would by thebe of enterocin interest to biosynthetic colleagues in naturalgene cluster product deletion discovery. (Figure 1a) and Strainconfirmed 172205 byDenc PCRwas (polymerase obtained by chain the enterocin reaction) biosynthetic amplification gene ( clusterSupplementary deletion(Figure Figure1 a)S1 and and confirmedTable2. S1 Results). by The PCR HPLC (polymerase profile of chain crude reaction) extract amplification in D.O. medium (Supplementary (Figure 1b) Figure showed S1 andthat Tableenterocin S1). Thebiosynthesis HPLCStrain profile were 172205Δ oftotally crudeenc blocked was extract obtained in in mutant D.O. by the medium strain enterocin 172205Δ (Figure biosyntheticenc1b), including showed gene cluster that its intermediate enterocindeletion (Figure biosynthesis metabolite 1a) - werecinnamic totallyand confirmedacid. blocked by in mutantPCR (polymerase strain 172205 chainD encreaction), including amplification its intermediate (Supplementary metabolite-cinnamic Figure S1 and acid. Table S1). The HPLC profile of crude extract in D.O. medium (Figure 1b) showed that enterocin biosynthesis were totally blocked in mutant strain 172205Δenc, including its intermediate metabolite- cinnamic acid. (a) (b) FigureFigure 1.1. ((aa)) TheThe organizationorganization(a) ofof enterocinenterocin biosyntheticbiosynthetic genegene clustercluster(b ) before before andand afterafter deletion.deletion. AmplificationAmplificationFigure 1. fragments fragments(a) The organization byby verifyingverifying of enterocin primersprimers werebiosyntheticwere labeledlabeled gene byby frontsclusterfronts inbeforein red; red; and ( b(b) ) HPLC afterHPLC deletion. detection detection of of crudecrude extractsAmplification extracts of of strain strain fragments 172205 172205 by wild verifyingwild type type primers and andD Δenc wereencin in D.O.labeled D.O. medium. medium.by fronts in red; (b) HPLC detection of crude extracts of strain 172205 wild type and Δenc in D.O. medium. AlmostAlmost 80 80 grams grams crude crude extract extract was was obtained obtained from from extraction extraction of 60 Lof fermentation 60 L fermentation broth of broth mutant of 172205mutantD enc172205ΔAlmostand
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