Culture-independent discovery of the malacidins as calcium-dependent antibiotics with activity against multidrug-resistant Gram-positive pathogens

Nature Microbiology

Volumn 3, Issue 4, 2018, Pages 415-422

  Hover, Bradley M ^a   Kim, Seong Hwan ^a   Katz, Micah ^a   Charlop Powers, Zachary ^a   Owen, Jeremy G ^a   Ternei, Melinda A ^a   Maniko, Jeffrey ^a   Estrela, Andreia B ^a   Molina, Henrik ^a   Park, Steven ^b   Perlin, David S ^b   Brady, Sean F ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; DAPTOMYCIN; MALACIDIN A; MALACIDIN B; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; CALCIUM; CYCLOPEPTIDE; LIPOPEPTIDE; MALACIDINS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG STRUCTURE; GRAM POSITIVE BACTERIUM; IN VIVO STUDY; MALE; MASS SPECTROMETRY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; RAT; SKIN INFECTION; SPRAGUE DAWLEY RAT; THIN LAYER CHROMATOGRAPHY; WOUND INFECTION; ANIMAL; CELL LINE; DRUG EFFECT; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; STAPHYLOCOCCUS INFECTION;

ANIMALS; ANTI-BACTERIAL AGENTS; CALCIUM; CELL LINE; DAPTOMYCIN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; HEK293 CELLS; HUMANS; LIPOPEPTIDES; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; PEPTIDES, CYCLIC; RATS; SOIL MICROBIOLOGY; STAPHYLOCOCCAL INFECTIONS;

EID: 85041902998     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/s41564-018-0110-1     Document Type: Article

References (30)

1. O'Neill, J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations (The Review on Antimicrobial Resistance, Wellcome Trust & UK Government, 2016).
2. Tringe, S. G. et al. Comparative metagenomics of microbial communities. Science 308, 554-557 (2005).
3. Reddy, B. V. et al. Natural product biosynthetic gene diversity in geographically distinct soil microbiomes. Appl. Environ. Microbiol. 78, 3744-3752 (2012).
4. Strieker, M. & Marahiel, M. A. The structural diversity of acidic lipopeptide antibiotics. ChemBioChem 10, 607-616 (2009).
5. Jung, D., Rozek, A., Okon, M. & Hancock, R. E. Structural transitions as determinants of the action of the calcium-dependent antibiotic daptomycin. Chem. Biol. 11, 949-957 (2004).
6. Bunkoczi, G., Vertesy, L. & Sheldrick, G. M. Structure of the lipopeptide antibiotic tsushimycin. Acta Crystallogr. Sect. D. 61, 1160-1164 (2005).
7. Katz, M., Hover, B. M. & Brady, S. F. Culture-independent discovery of natural products from soil metagenomes. J. Ind. Microbiol. Biotechnol. 43, 129-141 (2016).
8. Owen, J. G. et al. Mapping gene clusters within arrayed metagenomic libraries to expand the structural diversity of biomedically relevant natural products. Proc. Natl Acad. Sci. USA 110, 11797-11802 (2013).
9. Reddy, B. V., Milshteyn, A., Charlop-Powers, Z. & Brady, S. F. eSNaPD: a versatile, web-based bioinformatics platform for surveying and mining natural product biosynthetic diversity from metagenomes. Chem. Biol. 21, 1023-1033 (2014).
10. Brady, S. F. Construction of soil environmental DNA cosmid libraries and screening for clones that produce biologically active small molecules. Nat. Protoc. 2, 1297-1305 (2007).
11. Kim, J. H. et al. Cloning large natural product gene clusters from the environment: piecing environmental DNA gene clusters back together with TAR. Biopolymers 93, 833-844 (2010).
12. Silverman, J. A., Mortin, L. I., Vanpraagh, A. D., Li, T. & Alder, J. Inhibition of daptomycin by pulmonary surfactant: in vitro modeling and clinical impact. J. Infect. Dis. 191, 2149-2152 (2005).
13. Zhang, T., Taylor, S. D., Palmer, M. & Duhamel, J. Membrane binding and oligomerization of the lipopeptide A54145 studied by pyrene fluorescence. Biophys. J. 111, 1267-1277 (2016).
14. Straus, S. K. & Hancock, R. E. Mode of action of the new antibiotic for Gram-positive pathogens daptomycin: comparison with cationic antimicrobial peptides and lipopeptides. Biochim. Biophys. Acta 1758, 1215-1223 (2006).
15. Muller, A. et al. Daptomycin inhibits cell envelope synthesis by interfering with fluid membrane microdomains. Proc. Natl Acad. Sci. USA 113, E7077-E7086 (2016).
16. Schneider, T. et al. The lipopeptide antibiotic Friulimicin B inhibits cell wall biosynthesis through complex formation with bactoprenol phosphate. Antimicrob. Agents Ch. 53, 1610-1618 (2009).
17. Kleijn, L. H. et al. Total synthesis of Laspartomycin C and characterization of its antibacterial mechanism of action. J. Med. Chem. 59, 3569-3574 (2016).
18. Owen, J. G. et al. Multiplexed metagenome mining using short DNA sequence tags facilitates targeted discovery of epoxyketone proteasome inhibitors. Proc. Natl Acad. Sci. USA 112, 4221-4226 (2015).
19. Charlop-Powers, Z. et al. Urban park soil microbiomes are a rich reservoir of natural product biosynthetic diversity. Proc. Natl Acad. Sci. USA 113, 14811-14816 (2016).
20. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
21. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
22. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
23. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650 (2009).
24. Zhang, T., Luo, Y., Chen, Y., Li, X. & Yu, J. BIGrat: a repeat resolver for pyrosequencing-based re-sequencing with Newbler. BMC Res. Notes 5, 567 (2012).
25. Zhu, W., Lomsadze, A. & Borodovsky, M. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 38, e132 (2010).
26. Medema, M. H. et al. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 39, W339-W346 (2011).
27. Kallifidas, D. & Brady, S. F. Reassembly of functionally intact environmental DNA-derived biosynthetic gene clusters. Methods Enzymol. 517, 225-239 (2012).
28. Gietz, R. D. & Schiestl, R. H. Large-scale high-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2, 38-41 (2007).
29. Cockerill, F. R. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard-Ninth edition (Clinical and Laboratory Standards Institute, Wayne, PA, 2012).
30. Zhao, Y. et al. Carbohydrate-derived fulvic acid is a highly promising topical agent to enhance healing of wounds infected with drug-resistant pathogens. J. Trauma Acute Care Surg. 79, S121-S129 (2015).