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How the MccB bacterial ancestor of ubiquitin E1 initiates biosynthesis of the microcin C7 antibiotic.

Regni CA, Roush RF, Miller DJ, Nourse A, Walsh CT, Schulman BA
EMBO J 28 1953-64 (2009)
Related entries: 3h5a, 3h5r, 3h9g, 3h9j, 3h9q

Cited: 47 times
EuropePMC logo PMID: 19494832

Abstract

The 39-kDa Escherichia coli enzyme MccB catalyses a remarkable posttranslational modification of the MccA heptapeptide during the biosynthesis of microcin C7 (MccC7), a 'Trojan horse' antibiotic. The approximately 260-residue C-terminal region of MccB is homologous to ubiquitin-like protein (UBL) activating enzyme (E1) adenylation domains. Accordingly, MccB-catalysed C-terminal MccA-acyl-adenylation is reminiscent of the E1-catalysed activation reaction. However, unlike E1 substrates, which are UBLs with a C-terminal di-glycine sequence, MccB's substrate, MccA, is a short peptide with an essential C-terminal Asn. Furthermore, after an intramolecular rearrangement of MccA-acyl-adenylate, MccB catalyses a second, unique reaction, producing a stable phosphoramidate-linked analogue of acyl-adenylated aspartic acid. We report six-crystal structures of MccB in apo, substrate-, intermediate-, and inhibitor-bound forms. Structural and kinetic analyses reveal a novel-peptide clamping mechanism for MccB binding to heptapeptide substrates and a dynamic-active site for catalysing dual adenosine triphosphate-consuming reactions. The results provide insight into how a distinctive member of the E1 superfamily carries out two-step activation for generating the peptidyl-antibiotic MccC7.

Articles - 3h5n mentioned but not cited (3)

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Reviews citing this publication (10)

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  6. The Biochemistry and Structural Biology of Cyanobactin Pathways: Enabling Combinatorial Biosynthesis. Gu W, Dong SH, Sarkar S, Nair SK, Schmidt EW. Methods Enzymol 604 113-163 (2018)
  7. The structural biology of patellamide biosynthesis. Koehnke J, Bent AF, Houssen WE, Mann G, Jaspars M, Naismith JH. Curr Opin Struct Biol 29 112-121 (2014)
  8. Targeting adenylate-forming enzymes with designed sulfonyladenosine inhibitors. Lux MC, Standke LC, Tan DS. J Antibiot (Tokyo) 72 325-349 (2019)
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  10. Natural Trojan horse inhibitors of aminoacyl-tRNA synthetases. Travin DY, Severinov K, Dubiley S. RSC Chem Biol 2 468-485 (2021)

Articles citing this publication (34)

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  3. Expansion of ribosomally produced natural products: a nitrile hydratase- and Nif11-related precursor family. Haft DH, Basu MK, Mitchell DA. BMC Biol 8 70 (2010)
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  5. Structural Insights into Thioether Bond Formation in the Biosynthesis of Sactipeptides. Grove TL, Himes PM, Hwang S, Yumerefendi H, Bonanno JB, Kuhlman B, Almo SC, Bowers AA. J Am Chem Soc 139 11734-11744 (2017)
  6. Marine molecular machines: heterocyclization in cyanobactin biosynthesis. McIntosh JA, Schmidt EW. Chembiochem 11 1413-1421 (2010)
  7. Discovery of a new ATP-binding motif involved in peptidic azoline biosynthesis. Dunbar KL, Chekan JR, Cox CL, Burkhart BJ, Nair SK, Mitchell DA. Nat Chem Biol 10 823-829 (2014)
  8. Structures of the peptide-modifying radical SAM enzyme SuiB elucidate the basis of substrate recognition. Davis KM, Schramma KR, Hansen WA, Bacik JP, Khare SD, Seyedsayamdost MR, Ando N. Proc Natl Acad Sci U S A 114 10420-10425 (2017)
  9. Clostridiolysin S, a post-translationally modified biotoxin from Clostridium botulinum. Gonzalez DJ, Lee SW, Hensler ME, Markley AL, Dahesh S, Mitchell DA, Bandeira N, Nizet V, Dixon JE, Dorrestein PC. J Biol Chem 285 28220-28228 (2010)
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  12. MccE provides resistance to protein synthesis inhibitor microcin C by acetylating the processed form of the antibiotic. Novikova M, Kazakov T, Vondenhoff GH, Semenova E, Rozenski J, Metlytskaya A, Zukher I, Tikhonov A, Van Aerschot A, Severinov K. J Biol Chem 285 12662-12669 (2010)
  13. Nuclear Magnetic Resonance Structure and Binding Studies of PqqD, a Chaperone Required in the Biosynthesis of the Bacterial Dehydrogenase Cofactor Pyrroloquinoline Quinone. Evans RL, Latham JA, Xia Y, Klinman JP, Wilmot CM. Biochemistry 56 2735-2746 (2017)
  14. Comprehensive mapping of the Helicobacter pylori NikR regulon provides new insights in bacterial nickel responses. Vannini A, Pinatel E, Costantini PE, Pelliciari S, Roncarati D, Puccio S, De Bellis G, Peano C, Danielli A. Sci Rep 7 45458 (2017)
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  16. Observing the invisible through imaging mass spectrometry, a window into the metabolic exchange patterns of microbes. Gonzalez DJ, Xu Y, Yang YL, Esquenazi E, Liu WT, Edlund A, Duong T, Du L, Molnár I, Gerwick WH, Jensen PR, Fischbach M, Liaw CC, Straight P, Nizet V, Dorrestein PC. J Proteomics 75 5069-5076 (2012)
  17. Enzymatic synthesis of bioinformatically predicted microcin C-like compounds encoded by diverse bacteria. Bantysh O, Serebryakova M, Makarova KS, Dubiley S, Datsenko KA, Severinov K. mBio 5 e01059-14 (2014)
  18. Exploring the Post-translational Enzymology of PaaA by mRNA Display. Fleming SR, Himes PM, Ghodge SV, Goto Y, Suga H, Bowers AA. J Am Chem Soc 142 5024-5028 (2020)
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  20. Architecture of Microcin B17 Synthetase: An Octameric Protein Complex Converting a Ribosomally Synthesized Peptide into a DNA Gyrase Poison. Ghilarov D, Stevenson CEM, Travin DY, Piskunova J, Serebryakova M, Maxwell A, Lawson DM, Severinov K. Mol Cell 73 749-762.e5 (2019)
  21. Lasso Peptide Biosynthetic Protein LarB1 Binds Both Leader and Core Peptide Regions of the Precursor Protein LarA. Cheung WL, Chen MY, Maksimov MO, Link AJ. ACS Cent Sci 2 702-709 (2016)
  22. A Lanthipeptide-like N-Terminal Leader Region Guides Peptide Epimerization by Radical SAM Epimerases: Implications for RiPP Evolution. Fuchs SW, Lackner G, Morinaka BI, Morishita Y, Asai T, Riniker S, Piel J. Angew Chem Int Ed Engl 55 12330-12333 (2016)
  23. A Trojan-Horse Peptide-Carboxymethyl-Cytidine Antibiotic from Bacillus amyloliquefaciens. Serebryakova M, Tsibulskaya D, Mokina O, Kulikovsky A, Nautiyal M, Van Aerschot A, Severinov K, Dubiley S. J Am Chem Soc 138 15690-15698 (2016)
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