Discovery of phosphonic acid natural products by mining the genomes of 10,000 actinomycetes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 39, 2015, Pages 12175-12180

  Ju, Kou San ^a   Gao, Jiangtao ^a   Doroghazi, James R ^a   Wang, Kwo Kwang A ^a   Thibodeaux, Christopher J ^a   Li, Steven ^a   Metzger, Emily ^a   Fudala, John ^a   Su, Joleen ^a   Zhang, Jun Kai ^a,b   Lee, Jaeheon ^a   Cioni, Joel P ^a,b   Evans, Bradley S ^a   Hirota, Ryuichi ^a,c   Labeda, David P ^d   Van Der Donk, Wilfred A ^a   Metcalf, William W ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c HIROSHIMA UNIVERSITY   (Japan)

^d NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

Author keywords

Antibiotic; Genome mining; Natural products; Phosphonic acid

Indexed keywords

2,3 DIHYDROXYPROPYLPHOSPHONATE; ACETIC ACID DERIVATIVE; ESTER; N(G) HYDROXYARGININE; NATURAL PRODUCT; PHOSPHINOTHRICIN; PHOSPHONIC ACID DERIVATIVE; PHOSPHONOCYSTOXIMATE; UNCLASSIFIED DRUG; VALINE; BIOLOGICAL PRODUCT; PHOSPHOROUS ACID;

ACTINOBACTERIA; ARTICLE; BACILLUS CEREUS; BACTERIAL GENOME; BACTERIAL STRAIN; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE CLUSTER; GENE SEQUENCE; GENETIC SCREENING; GENOME ANALYSIS; GENOME MINING; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PHOSPHORYLATION; PRIORITY JOURNAL; STREPTOMYCES HYGROSCOPICUS; THERMODYNAMICS; CHEMISTRY; DNA SEQUENCE; DRUG DEVELOPMENT; GENE LIBRARY; GENETICS; GENOMICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROCEDURES; TRENDS;

ACTINOBACTERIA; BASE SEQUENCE; BIOLOGICAL PRODUCTS; DRUG DISCOVERY; GENE LIBRARY; GENOME, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE DATA; PHOSPHOROUS ACIDS; SEQUENCE ANALYSIS, DNA;

EID: 84942930937     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1500873112     Document Type: Article

References (49)

1. Cragg GM, Newman DJ (2013) Natural products: A continuing source of novel drug leads. Biochim Biophys Acta 1830(6):3670-3695.
2. Koehn FE, Carter GT (2005) The evolving role of natural products in drug discovery. Nat Rev Drug Discov 4(3):206-220.
3. Brötz-Oesterhelt H, Sass P (2010) Postgenomic strategies in antibacterial drug discovery. Future Microbiol 5(10):1553-1579.
4. Baltz RH (2006) Marcel Faber Roundtable: Is our antibiotic pipeline unproductive because of starvation, constipation or lack of inspiration? J Ind Microbiol Biotechnol 33(7):507-513.
5. Bachmann BO, Van Lanen SG, Baltz RH (2014) Microbial genome mining for accelerated natural products discovery: Is a renaissance in the making? J Ind Microbiol Biotechnol 41(2):175-184.
6. Challis GL (2008) Genome mining for novel natural product discovery. J Med Chem 51(9):2618-2628.
7. Bode HB, Müller R (2005) The impact of bacterial genomics on natural product research. Angew Chem Int Ed Engl 44(42):6828-6846.
8. Zettler J, et al. (2014) New aminocoumarins from the rare actinomycete Catenulispora acidiphila DSM 44928: Identification, structure elucidation, and heterologous production. ChemBioChem 15(4):612-621.
9. Pidot S, Ishida K, Cyrulies M, Hertweck C (2014) Discovery of clostrubin, an exceptional polyphenolic polyketide antibiotic from a strictly anaerobic bacterium. Angew Chem Int Ed Engl 53(30):7856-7859.
10. Craig JW, Chang FY, Kim JH, Obiajulu SC, Brady SF (2010) Expanding small-molecule functional metagenomics through parallel screening of broad-host-range cosmid environmental DNA libraries in diverse proteobacteria. Appl Environ Microbiol 76(5):1633-1641.
11. Owen JG, et al. (2013) Mapping gene clusters within arrayed metagenomic libraries to expand the structural diversity of biomedically relevant natural products. Proc Natl Acad Sci USA 110(29):11797-11802.
12. Chang FY, Brady SF (2013) Discovery of indolotryptoline antiproliferative agents by homology-guided metagenomic screening. Proc Natl Acad Sci USA 110(7):2478-2483.
13. Abdelmohsen UR, et al. (2015) Elicitation of secondary metabolism in actinomycetes. Biotechnol Adv, 10.1016/j.biotechadv. 2015.06.003.
14. Luo Y, Cobb RE, Zhao H (2014) Recent advances in natural product discovery. Curr Opin Biotechnol 30:230-237.
15. Metcalf WW, van der Donk WA (2009) Biosynthesis of phosphonic and phosphinic acid natural products. Annu Rev Biochem 78:65-94.
16. Bérdy J (2012) Thoughts and facts about antibiotics: Where we are now and where we are heading. J Antibiot (Tokyo) 65(8):385-395.
17. Ju KS, Doroghazi JR, Metcalf WW (2014) Genomics-enabled discovery of phosphonate natural products and their biosynthetic pathways. J Ind Microbiol Biotechnol 41(2):345-356.
18. Eliot AC, et al. (2008) Cloning, expression, and biochemical characterization of Streptomyces rubellomurinus genes required for biosynthesis of antimalarial compound FR900098. Chem Biol 15(8):765-770.
19. Blodgett JA, Zhang JK, Metcalf WW (2005) Molecular cloning, sequence analysis, and heterologous expression of the phosphinothricin tripeptide biosynthetic gene cluster from Streptomyces viridochromogenes DSM 40736. Antimicrob Agents Chemother 49(1):230-240.
20. Woodyer RD, et al. (2006) Heterologous production of fosfomycin and identification of the minimal biosynthetic gene cluster. Chem Biol 13(11):1171-1182.
21. Borisova SA, Circello BT, Zhang JK, van der Donk WA, Metcalf WW (2010) Biosynthesis of rhizocticins, antifungal phosphonate oligopeptides produced by Bacillus subtilis ATCC6633. Chem Biol 17(1):28-37.
22. Circello BT, Miller CG, Lee JH, van der Donk WA, Metcalf WW (2011) The antibiotic dehydrophos is converted to a toxic pyruvate analog by peptide bond cleavage in Salmonella enterica. Antimicrob Agents Chemother 55(7):3357-3362.
23. Yu X, et al. (2013) Diversity and abundance of phosphonate biosynthetic genes in nature. Proc Natl Acad Sci USA 110(51):20759-20764.
24. Evans BS, et al. (2013) Discovery of the antibiotic phosacetamycin via a new mass spectrometry-based method for phosphonic acid detection. ACS Chem Biol 8(5):908-913.
25. Nielsen ML, Pustinger JV, Strobel J (1964) Phosphorus-31 nuclear magnetic resonance chemical shifts of phosphorus compounds. J Chem Eng Data 9:167-170.
26. Takahashi E, Kimura T, Nakamura K, Arahira M, Iida M (1995) Phosphonothrixin, a novel herbicidal antibiotic produced by Saccharothrix sp. ST-888. I. Taxonomy, fermentation, isolation and biological properties. J Antibiot (Tokyo) 48(10):1124-1129.
27. Okuhara M, et al. (1980) Studies on new phosphonic acid antibiotics. I. FR-900098, isolation and characterization. J Antibiot (Tokyo) 33(1):13-17.
28. Okuhara M, et al. (1980) Studies on new phosphonic acid antibiotics. III. Isolation and characterization of FR-31564, FR-32863 and FR-33289. J Antibiot (Tokyo) 33(1):24-28.
29. Krug D, Müller R (2014) Secondary metabolomics: The impact of mass spectrometrybased approaches on the discovery and characterization of microbial natural products. Nat Prod Rep 31(6):768-783.
30. Forseth RR, Schroeder FC (2011) NMR-spectroscopic analysis of mixtures: From structure to function. Curr Opin Chem Biol 15(1):38-47.
31. Lin J, Nishiyama M, Kuzuyama T (2015) Identification of the biosynthetic gene cluster for the herbicide phosphonothrixin in Saccharothrix sp. ST-888. J Antibiot (Tokyo) 68(5):357-359.
32. Blodgett JA, et al. (2007) Unusual transformations in the biosynthesis of the antibiotic phosphinothricin tripeptide. Nat Chem Biol 3(8):480-485.
33. Hove-Jensen B, Zechel DL, Jochimsen B (2014) Utilization of glyphosate as phosphate source: Biochemistry and genetics of bacterial carbon-phosphorus lyase. Microbiol Mol Biol Rev 78(1):176-197.
34. Maehr H, Blount JF, Pruess DL, Yarmchuk L, Kellett M (1973) Antimetabolites produced by microorganisms. 8. N5-hydroxy-L-arginine, a new naturally occurring amino acid. J Antibiot (Tokyo) 26(5):284-288.
35. Perlman D, Vlietinck AJ, Matthews HW, Lo FF (1974) Microbial production of vitamin B12 antimetabolites. I. N5-hydroxy-L-arginine from Bacillus cereus 439. J Antibiot (Tokyo) 27(11):826-832.
36. Fischer B, et al. (1973) [Metabolic products of microorganisms. 118. Delta-N-hydroxy-L-arginine, an amino acid antagonist from Nannizzia gypsea]. Arch Mikrobiol 91(3):203-220. German.
37. Bougioukou DJ, Mukherjee S, van der Donk WA (2013) Revisiting the biosynthesis of dehydrophos reveals a tRNA-dependent pathway. Proc Natl Acad Sci USA 110(27):10952-10957.
38. Gao J, et al. (2014) Use of a phosphonate methyltransferase in the identification of the fosfazinomycin biosynthetic gene cluster. Angew Chem Int Ed Engl 53(5):1334-1337.
39. Atherton FR, et al. (1982) Antibacterial activity and mechanism of action of phosphonopeptides based on aminomethylphosphonic acid. Antimicrob Agents Chemother 22(4):571-578.
40. Cioni JP, et al. (2014) Cyanohydrin phosphonate natural product from Streptomyces regensis. J Nat Prod 77(2):243-249.
41. Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303-333.
42. Hakala MT, Glaid AJ, Schwert GW (1956) Lactic dehydrogenase. II. Variation of kinetic and equilibrium constants with temperature. J Biol Chem 221(1):191-209.
43. Philmus B, Guerrette JP, Hemscheidt TK (2009) Substrate specificity and scope of MvdD, a GRASP-like ligase from the microviridin biosynthetic gene cluster. ACS Chem Biol 4(6):429-434.
44. Seto H, et al. (1983) Studies on the biosynthesis of bialaphos (SF-1293). 2. Isolation of the first natural products with a C-P-H bond and their involvement in the C-P-C bond formation. J Antibiot (Tokyo) 36(1):96-98.
45. Yu X, Price NP, Evans BS, Metcalf WW (2014) Purification and characterization of phosphonoglycans from Glycomyces sp. strain NRRL B-16210 and Stackebrandtia nassauensis NRRL B-16338. J Bacteriol 196(9):1768-1779.
46. Doroghazi JR, et al. (2014) A roadmap for natural product discovery based on largescale genomics and metabolomics. Nat Chem Biol 10(11):963-968.
47. Doroghazi JR, et al. (2011) Genome sequences of three tunicamycin-producing Streptomyces Strains, S. chartreusis NRRL 12338, S. chartreusis NRRL 3882, and S. lysosuperificus ATCC 31396. J Bacteriol 193(24):7021-7022.
48. Hyatt D, et al. (2010) Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119.
49. Peng Y, Leung HC, Yiu SM, Chin FY (2012) IDBA-UD: A de novo assembler for singlecell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28(11):1420-1428.