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Download (831Kb) Kent Academic Repository Full text document (pdf) Citation for published version Wichner, Dominik and Idris, Hamidah and Houssen, Wael E and McEwan, Andrew R and Bull, Alan T. and Asenjo, Juan A and Goodfellow, Michael and Jaspars, Marcel and Ebel, Rainer and Rateb, Mostafa E (2016) Isolation and anti-HIV-1 integrase activity of lentzeosides A–F from extremotolerant lentzea sp. H45, a strain isolated from a high-altitude Atacama Desert soil. The DOI https://doi.org/10.1038/ja.2016.78 Link to record in KAR https://kar.kent.ac.uk/61946/ Document Version Author's Accepted Manuscript Copyright & reuse Content in the Kent Academic Repository is made available for research purposes. Unless otherwise stated all content is protected by copyright and in the absence of an open licence (eg Creative Commons), permissions for further reuse of content should be sought from the publisher, author or other copyright holder. Versions of research The version in the Kent Academic Repository may differ from the final published version. Users are advised to check http://kar.kent.ac.uk for the status of the paper. Users should always cite the published version of record. Enquiries For any further enquiries regarding the licence status of this document, please contact: [email protected] If you believe this document infringes copyright then please contact the KAR admin team with the take-down information provided at http://kar.kent.ac.uk/contact.html 1 Isolation and Anti-HIV-1 Integrase Activity of Lentzeosides A-F from Extremotolerant 2 Lentzea sp. H45, a strain isolated from a high altitude Atacama Desert soil 3 Running head: Lentzeosides A-F from Extremotolerant Lentzea sp. H45 1,9 2 1,4,8 1,4 5 4 Dominik Wichner, Hamidah Idris, Wael E. Houssen, Andrew R. McEwan, Alan T. Bull, 5 Juan A. Asenjo, 7 Michael Goodfellow, 2 Marcel Jaspars, 1 Rainer Ebel,1 and Mostafa E. Rateb, 1,3,6,* 6 1 Marine Biodiscovery Centre, University of Aberdeen, Aberdeen AB24 3UE, Scotland, UK. 7 2 School of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, UK. 8 3 School of Science & Sport, University of the West of Scotland, Paisley PA1 2BE, UK. 9 4 Institute of Medical Sciences, University of Aberdeen, Aberdeen AB25 2ZD, Scotland, UK. 10 5 School of Biosciences, University of Kent, Canterbury, Kent CT2 7NJ, U.K. 11 6 Pharmacognosy Department, School of Pharmacy, Beni-Suef University, Beni-Suef 32514, Egypt. 12 7 Centre for Biotechnology and Bioengineering (CeBiB), Department of Chemical Engineering and 13 Biotechnology, Universidad de Chile, Beauchef 851, Santiago 8370450, Chile. 14 8 Pharmacognosy Department, Faculty of Pharmacy, Mansoura University, Mansoura 35516, Egypt. 15 9 University of Regensburg, Universitätsstraße 31, Regensburg 93053, Germany. 16 17 18 The extremotolerant isolate H45 was one of several actinomycetes isolated from a high altitude 19 Atacama Desert soil collected in northwest Chile. The isolate was identified as a new Lentzea sp. 20 using a combination of chemotaxonomic, morphological and phylogenetic properties. Large scale 21 fermentation of the strain in two different media followed by chromatographic purification led to 22 the isolation of six new diene and monoene glycosides named lentzeosides A–F, together with the 23 known compound (Z)-3-hexenyl glucoside. The structures of the new compounds were confirmed 24 by HRESIMS and NMR analyses. Compounds 1-6 displayed moderate inhibitory activity against 25 HIV integrase. 26 * Correspondence : Mostafa E. Rateb, E-mail: [email protected], Tel: +4414418483072 1 1 INTRODUCTION 2 Natural products are known to be a rich source of diverse chemical scaffolds for drug discovery. 3 However, their use has diminished in the past two decades, mainly due to technical barriers when 4 screening natural products in high-throughput assays against molecular targets and to their limited 5 availability for clinical trials.1 Additionally, the discovery of new bioactive natural products is 6 challenging due to the high rate of re-discovery of known metabolites, a problem that can be 7 addressed by isolating and screening novel microorganisms from underexplored habitats, such as 8 desert biomes 2,3 , and by incorporating rigorous dereplication procedures into all stages of the 9 discovery process. In addition, industry has realized that phenotypic screening is more effective at 10 discovering new bioactive compounds than narrow screening of molecular targets. 11 The Atacama Desert in Chile is known for its extreme aridity which has persisted for at least ∼15 12 million years. 4 Some regions in the desert were once thought to have “Mars-like” soils deemed too 13 extreme for life to exist given high levels of UV radiation, the presence of inorganic oxidants, areas 14 of high salinity, and very low concentrations of organic carbon.5 However, recent research has 15 revealed extraordinary bacterial diversity across a range of Atacama environments 6,7 , and many 16 novel actinomycetes have been isolated from hyper – and extreme hyper-arid soils.8,9 Biological 17 and genome-guided screening of some of these actinomycetes has led to the isolation and 18 characterization of new natural products belonging to diverse structural classes and exhibiting 19 various biological activities, as exemplified by the antimicrobial chaxamycins and chaxalactins 20 isolated from Streptomyces leeuwenhoekii C34 T, the abenquines from Streptomyces sp. DB634, the 21 antitumor atacamycins from Streptomyces sp. C38, and the cell invasion inhibitor chaxapeptin from 22 S. leeuwenhoekii strain C58.10-16 2 1 As part of our ongoing program to investigate the extremobiosphere as a source of new natural 2 products, we have focused our attention on Lentzea sp. strain H45 which was isolated from a high 3 altitude Atacama Desert soil and shown to produce a specific pattern of secondary metabolites 4 based on its LCMS profile and associated NMR data. Chemical screening of the strain on two 5 different cultivation media led to the isolation of six new and one known diene, as well as monoene 6 glycosides (Figure 1). Structure elucidation of these compounds was based on HRESIMS, 1D and 7 2D NMR analyses. The isolated compounds were screened for their inhibitory activity against HIV- 8 1 integrase, an enzyme that is critical for the integration of the HIV genome into the host genome.17 9 This target is very attractive for the development of new anti-HIV therapy as it is selective for the 10 virus. 11 RESULTS 12 In this study, actinobacterial isolate H45 was obtained from subsurface soil sample collected at an 13 altitude > 5000 m in the vicinity of the ALMA Observatory in the Atacama Desert, Chile. The 14 chemotaxonomic, morphological, physiological and phylogenetic properties of strain H45 are in 15 line with its classification in the genus Lentzea .18,19 The strain was found to be an aerobic, Gram- 16 positive actinomycete that formed a branched substrate mycelium and aerial hyphae that 17 fragmented into rod-shaped elements (Figure 2), while chemical analysis of whole-organism 18 hydrolysates revealed the presence of meso -diaminopimelic acid and galactose, mannose and 19 ribose, and the predominant isoprenologue was tetrahydrogenated menaquinone with nine isoprene 20 units (MK9[H4]). The organism formed a distinct branch at the periphery of the Lentzea 16S rRNA 21 gene tree, a position that was supported by all of the tree-making algorithms and by a 69% bootstrap 22 value (Figure 3). The strain was most closely, albeit loosely, related to Lentzea kentuckyensis T 3 1 NRRL B-34416. These results clearly show that the isolate forms a new centre of taxonomic 2 variation in the genus Lentzea consistent with its recognition as a putative new species. 3 Large scale fermentation of Lentzea sp. strain H45 on two different media supplemented with 4 Diaion HP-20 resin was followed by methanolic extraction of the resin beads; subsequently, the 5 crude extract was subject to multiple steps of medium and high pressure preparative C-18 6 chromatography which resulted in the isolation of six new and one known natural product based 7 on HRESIMS and NMR data (Figure 1). 8 HRESIMS analysis of compound 1 yielded a [M+Na] + ion at m/z 281.1351 indicating a molecular 1 13 9 formula of C 13 H22 O5. The analysis of H, C and multiplicity-edited HSQC NMR spectra revealed 10 the presence of one methylene ( δC/δH 20.5/2.16) and one oxymethylene group ( δC/δH 68.3/4.26, 11 4.08), one methyl doublet (δC/δH 17.9/1.15), one methyl triplet (δC/δH 14.2/0.94), four olefinic 12 resonances ( δC/δH 133.7/5.42, 129.6/5.71, 127.4/5.94, 127.0/6.58) and five oxymethine groups 1 13 (δC/δH 102.1/4.15, 76.4/3.09, 75.3/2.80, 73.7/2.98, 71.5/3.15). Furthermore, the H NMR spectrum 14 showed 3 hydroxy groups resonating at δH 4.8-5.1. The COSY correlations of H 2-1 through H3-7 15 indicated a spin system comprising two conjugated olefins with a terminal ethyl group and 16 established a (2 E,4 Z)-heptadien-1-ol substructure (Figure 4). This was corroborated by the HMBC 17 correlations of H2-1/C-3, H-2/C-4, and H 3-7 to both C-5 and C-6 (Figure 4). The COSY spectrum 18 indicated a second spin system which included the signals H-1' to H3-6', which in combination with 19 the HMBC correlation of H-1'/C-5' suggested a β-L-quinovopyranose (β-L-6- 20 deoxyglucopyranose), which was confirmed by the optical rotation, the coupling constant of the 21 anomeric proton ( J = 7.8 Hz), axial-axial proton couplings for H1'/H2', H2'/H3', H3'/H4', H4'/H5' 22 (Table 2) as well as the agreement of the 13 C NMR data and the ROESY correlations with reported 23 data.
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