Genome Mining of the Marine Actinomycete Sp. DUT11 and Discovery of Tunicamycins As Anti-complement Agents

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2018 Jul 6

PMID 29973921

Citations 11

Authors

Xiao-Na Xu

Liang-Yu Chen

Chao Chen

Ya-Jie Tang

Feng-Wu Bai

Chun Su

Xin-Qing Zhao

Affiliations

Soon will be listed here.

Abstract

Marine actinobacteria are potential producers of various secondary metabolites with diverse bioactivities. Among various bioactive compounds, anti-complement agents have received great interest for drug discovery to treat numerous diseases caused by inappropriate activation of the human complement system. However, marine streptomycetes producing anti-complement agents are still poorly explored. In this study, a marine-derived strain sp. DUT11 showing superior anti-complement activity was focused, and its genome sequence was analyzed. Gene clusters showing high similarities to that of tunicamycin and nonactin were identified, and their corresponding metabolites were also detected. Subsequently, tunicamycin I, V, and VII were isolated from sp. DUT11. Anti-complement assay showed that tunicamycin I, V, VII inhibited complement activation through the classic pathway, whereas no anti-complement activity of nonactin was detected. This is the first time that tunicamycins are reported to have such activity. In addition, genome analysis indicates that sp. DUT11 has the potential to produce novel lassopeptides and lantibiotics. These results suggest that marine are rich sources of anti-complement agents for drug discovery.

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References

Blodgett J, Oh D, Cao S, Currie C, Kolter R, Clardy J . Common biosynthetic origins for polycyclic tetramate macrolactams from phylogenetically diverse bacteria. Proc Natl Acad Sci U S A. 2010; 107(26):11692-7. PMC: 2900643. DOI: 10.1073/pnas.1001513107. View

Lee Y, Kim H, Liu C, Lee H . A simple method for DNA extraction from marine bacteria that produce extracellular materials. J Microbiol Methods. 2002; 52(2):245-50. DOI: 10.1016/s0167-7012(02)00180-x. View

Ye S, Molloy B, Brana A, Zabala D, Olano C, Cortes J . Identification by Genome Mining of a Type I Polyketide Gene Cluster from Involved in the Biosynthesis of Pyridine and Piperidine Alkaloids Argimycins P. Front Microbiol. 2017; 8:194. PMC: 5300972. DOI: 10.3389/fmicb.2017.00194. View

Li W, Xu P, Schumann P, Zhang Y, Pukall R, Xu L . Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China), and emended description of the genus Georgenia. Int J Syst Evol Microbiol. 2007; 57(Pt 7):1424-1428. DOI: 10.1099/ijs.0.64749-0. View

Wang L, Zhang H, Zhang X, Chen Z . Purification and identification of a novel heteropolysaccharide RBPS2a with anti-complementary activity from defatted rice bran. Food Chem. 2015; 110(1):150-5. DOI: 10.1016/j.foodchem.2008.01.041. View

Martinez-Haya B, Aviles-Moreno J, Hamad S, Elguero J . On the ionophoric selectivity of nonactin and related macrotetrolide derivatives. Phys Chem Chem Phys. 2016; 19(2):1288-1297. DOI: 10.1039/c6cp05324f. View

Kim O, Cho Y, Lee K, Yoon S, Kim M, Na H . Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol. 2011; 62(Pt 3):716-721. DOI: 10.1099/ijs.0.038075-0. View

Ueda K, Oinuma K, Ikeda G, Hosono K, Ohnishi Y, Horinouchi S . AmfS, an extracellular peptidic morphogen in Streptomyces griseus. J Bacteriol. 2002; 184(5):1488-92. PMC: 134859. DOI: 10.1128/JB.184.5.1488-1492.2002. View

Chen W, Qu D, Zhai L, Tao M, Wang Y, Lin S . Characterization of the tunicamycin gene cluster unveiling unique steps involved in its biosynthesis. Protein Cell. 2010; 1(12):1093-105. PMC: 4875072. DOI: 10.1007/s13238-010-0127-6. View

10.

Coppola-Segovia V, Cavarsan C, Maia F, Ferraz A, Nakao L, Lima M . ER Stress Induced by Tunicamycin Triggers α-Synuclein Oligomerization, Dopaminergic Neurons Death and Locomotor Impairment: a New Model of Parkinson's Disease. Mol Neurobiol. 2016; 54(8):5798-5806. DOI: 10.1007/s12035-016-0114-x. View

11.

Prieto-Davo A, Dias T, Gomes S, Rodrigues S, Parera-Valadez Y, Borralho P . The Madeira Archipelago As a Significant Source of Marine-Derived Actinomycete Diversity with Anticancer and Antimicrobial Potential. Front Microbiol. 2016; 7:1594. PMC: 5053986. DOI: 10.3389/fmicb.2016.01594. View

12.

Walczak R, Woo A, Strohl W, Priestley N . Nonactin biosynthesis: the potential nonactin biosynthesis gene cluster contains type II polyketide synthase-like genes. FEMS Microbiol Lett. 2000; 183(1):171-5. DOI: 10.1111/j.1574-6968.2000.tb08953.x. View

13.

Lee I, Kim Y, Park S, Chun J . OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol. 2015; 66(2):1100-1103. DOI: 10.1099/ijsem.0.000760. View

14.

Yin X, Lu Y, Cheng Z, Chen D . Anti-Complementary Components of Helicteres angustifolia. Molecules. 2016; 21(11). PMC: 6273495. DOI: 10.3390/molecules21111506. View

15.

Maksimov M, Pan S, Link A . Lasso peptides: structure, function, biosynthesis, and engineering. Nat Prod Rep. 2012; 29(9):996-1006. DOI: 10.1039/c2np20070h. View

16.

Xu Z, Hao B . CVTree update: a newly designed phylogenetic study platform using composition vectors and whole genomes. Nucleic Acids Res. 2009; 37(Web Server issue):W174-8. PMC: 2703908. DOI: 10.1093/nar/gkp278. View

17.

Patzer S, Braun V . Gene cluster involved in the biosynthesis of griseobactin, a catechol-peptide siderophore of Streptomyces sp. ATCC 700974. J Bacteriol. 2009; 192(2):426-35. PMC: 2805312. DOI: 10.1128/JB.01250-09. View

18.

Berlin K, Koren S, Chin C, Drake J, Landolin J, Phillippy A . Assembling large genomes with single-molecule sequencing and locality-sensitive hashing. Nat Biotechnol. 2015; 33(6):623-30. DOI: 10.1038/nbt.3238. View

19.

Carver T, Harris S, Berriman M, Parkhill J, McQuillan J . Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics. 2011; 28(4):464-9. PMC: 3278759. DOI: 10.1093/bioinformatics/btr703. View

20.

Zhang Y, Huang H, Xu S, Wang B, Ju J, Tan H . Activation and enhancement of Fredericamycin A production in deepsea-derived Streptomyces somaliensis SCSIO ZH66 by using ribosome engineering and response surface methodology. Microb Cell Fact. 2015; 14:64. PMC: 4425903. DOI: 10.1186/s12934-015-0244-2. View