Published:26 May 2021https://doi.org/10.1098/rsob.200386
References
- 1. Cragg GM, Newman DJ. 2013 Natural products: a continuing source of novel drug leads. Biochim. Biophys. Acta. 1830, 3670-3695. (doi:10.1016/j.bbagen.2013.02.008) Crossref, PubMed, Web of Science, Google Scholar
- 2. Felnagle EA, Jackson EE, Chan YA, Podevels AM, Berti AD, McMahon MD, Thomas MG. 2008 Nonribosomal peptide synthetases involved in the production of medically relevant natural products. Mol. Pharm. 5, 191-211. (doi:10.1021/mp700137g) Crossref, PubMed, Web of Science, Google Scholar
- 3. Galm U, Wendt-Pienkowski E, Wang L, Huang S-X, Unsin C, Tao M, Coughlin JM, Shen B. 2011 Comparative analysis of the biosynthetic gene clusters and pathways for three structurally related antitumor antibiotics: bleomycin, tallysomycin, and zorbamycin. J. Nat. Prod. 74, 526-536. (doi:10.1021/np1008152) Crossref, PubMed, Web of Science, Google Scholar
- 4. Menkhaus M, Ullrich C, Kluge B, Vater J, Vollenbroich D, Kamp RM. 1993 Structural and functional organization of the surfactin synthetase multienzyme system. J. Biol. Chem. 268, 7678-7684. (doi:10.1016/S0021-9258(18)53010-6) Crossref, PubMed, Web of Science, Google Scholar
- 5. Singh M, Chaudhary S, Sareen D. 2017 Non-ribosomal peptide synthetases: identifying the cryptic gene clusters and decoding the natural product. J. Biosci. 42, 175-187. (doi:10.1007/s12038-017-9663-z) Crossref, PubMed, Web of Science, Google Scholar
- 6. Gulick AM. 2017 Nonribosomal peptide synthetase biosynthetic clusters of ESKAPE pathogens. Nat. Prod. Rep. 34, 981-1009. (doi:10.1039/C7NP00029D) Crossref, PubMed, Web of Science, Google Scholar
- 7. Vassaux A, Meunier L, Vandenbol M, Baurain D, Fickers P, Jacques P, Leclère V. 2019 Nonribosomal peptides in fungal cell factories: from genome mining to optimized heterologous production. Biotechnol. Adv. 37, 107449. (doi:10.1016/j.biotechadv.2019.107449) Crossref, PubMed, Web of Science, Google Scholar
- 8. Izoré T, Cryle MJ. 2018 The many faces and important roles of protein-protein interactions during non-ribosomal peptide synthesis. Nat. Prod. Rep. 35, 1120-1139. (doi:10.1039/C8NP00038G) Crossref, PubMed, Web of Science, Google Scholar
- 9. Jaremko MJ, Davis TD, Corpuz JC, Burkart MD. 2020 Type II non-ribosomal peptide synthetase proteins: structure, mechanism, and protein-protein interactions. Nat. Prod. Rep. 37, 355-379. (doi:10.1039/C9NP00047J) Crossref, PubMed, Web of Science, Google Scholar
- 10. Hertweck C. 2009 The biosynthetic logic of polyketide diversity. Angew Chem. Int. Ed. Engl. 48, 4688-4716. (doi:10.1002/anie.200806121) Crossref, PubMed, Web of Science, Google Scholar
- 11. Miyanaga A, Kudo F, Eguchi T. 2018 Protein-protein interactions in polyketide synthase-nonribosomal peptide synthetase hybrid assembly lines. Nat. Prod. Rep. 35, 1185-1209. (doi:10.1039/C8NP00022K) Crossref, PubMed, Web of Science, Google Scholar
- 12. Crosby J, Crump MP. 2012 The structural role of the carrier protein–active controller or passive carrier. Nat. Prod. Rep. 29, 1111-1137. (doi:10.1039/c2np20062g) Crossref, PubMed, Web of Science, Google Scholar
- 13. Koglin A 2006 Conformational switches modulate protein interactions in peptide antibiotic synthetases. Science 312, 273-276. (doi:10.1126/science.1122928) Crossref, PubMed, Web of Science, Google Scholar
- 14. Frueh DP, Arthanari H, Koglin A, Vosburg DA, Bennett AE, Walsh CT, Wagner G. 2008 Dynamic thiolation-thioesterase structure of a non-ribosomal peptide synthetase. Nature 454, 903-906. (doi:10.1038/nature07162) Crossref, PubMed, Web of Science, Google Scholar
- 15. Jaremko MJ, Lee DJ, Opella SJ, Burkart MD. 2015 Structure and substrate sequestration in the Pyoluteorin type II peptidyl carrier protein PltL. J. Am. Chem. Soc. 137, 11 546-11 549. (doi:10.1021/jacs.5b04525) Crossref, Web of Science, Google Scholar
- 16. Beld J, Sonnenschein EC, Vickery CR, Noel JP, Burkart MD. 2014 The phosphopantetheinyl transferases: catalysis of a post-translational modification crucial for life. Nat. Prod. Rep. 31, 61-108. (doi:10.1039/C3NP70054B) Crossref, PubMed, Web of Science, Google Scholar
- 17. Pfeifer BA, Admiraal SJ, Gramajo H, Cane DE, Khosla C. 2001 Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli. Science 291, 1790-1792. (doi:10.1126/science.1058092) Crossref, PubMed, Web of Science, Google Scholar
- 18. Gulick AM, Aldrich CC. 2018 Trapping interactions between catalytic domains and carrier proteins of modular biosynthetic enzymes with chemical probes. Nat. Prod. Rep. 35, 1156-1184. (doi:10.1039/C8NP00044A) Crossref, PubMed, Web of Science, Google Scholar
- 19. Reimer JM, Aloise MN, Harrison PM, Schmeing TM. 2016 Synthetic cycle of the initiation module of a formylating nonribosomal peptide synthetase. Nature 529, 239-242. (doi:10.1038/nature16503) Crossref, PubMed, Web of Science, Google Scholar
- 20. Drake EJ, Miller BR, Shi C, Tarrasch JT, Sundlov JA, Allen CL, Skiniotis G, Aldrich CC, Gulick AM. 2016 Structures of two distinct conformations of holo-non-ribosomal peptide synthetases. Nature 529, 235-238. (doi:10.1038/nature16163) Crossref, PubMed, Web of Science, Google Scholar
- 21. Tarry MJ, Haque AS, Bui KH, Schmeing TM. 2017 X-Ray crystallography and electron microscopy of cross- and multi-module nonribosomal peptide synthetase proteins reveal a flexible architecture. Structure 25, 783-793.e4. (doi:10.1016/j.str.2017.03.014) Crossref, PubMed, Web of Science, Google Scholar
- 22. Reimer JM, Eivaskhani M, Harb I, Guarné A, Weigt M, Schmeing TM. 2019 Structures of a dimodular nonribosomal peptide synthetase reveal conformational flexibility. Science 366, eaaw4388. (doi:10.1126/science.aaw4388) Crossref, PubMed, Web of Science, Google Scholar
- 23. Kudo F, Miyanaga A, Eguchi T. 2019 Structural basis of the nonribosomal codes for nonproteinogenic amino acid selective adenylation enzymes in the biosynthesis of natural products. J. Ind. Microbiol. Biotechnol. 46, 515-536. (doi:10.1007/s10295-018-2084-7) Crossref, PubMed, Web of Science, Google Scholar
- 24. Walsh CT, Chen H, Keating TA, Hubbard BK, Losey HC, Luo L, Marshall CG, Miller DA, Patel HM. 2001 Tailoring enzymes that modify nonribosomal peptides during and after chain elongation on NRPS assembly lines. Curr. Opin. Chem. Biol. 5, 525-534. (doi:10.1016/S1367-5931(00)00235-0) Crossref, PubMed, Web of Science, Google Scholar
- 25. Tseng CC, Bruner SD, Kohli RM, Marahiel MA, Walsh CT, Sieber SA. 2002 Characterization of the surfactin synthetase C-terminal thioesterase domain as a cyclic depsipeptide synthase. Biochemistry 41, 13 350-13 359. (doi:10.1021/bi026592a) Crossref, Web of Science, Google Scholar
- 26. Bruner SD, Weber T, Kohli RM, Schwarzer D, Marahiel MA, Walsh CT, Stubbs MT. 2002 Structural basis for the cyclization of the lipopeptide antibiotic surfactin by the thioesterase domain SrfTE. Structure 10, 301-310. (doi:10.1016/S0969-2126(02)00716-5) Crossref, PubMed, Web of Science, Google Scholar
- 27. Alonzo DA, Schmeing TM. 2020 Biosynthesis of depsipeptides, or Depsi: the peptides with varied generations. Protein Sci. 29, 2316-2347. (doi:10.1002/pro.3979) Crossref, PubMed, Web of Science, Google Scholar
- 28. Miller BR, Drake EJ, Shi C, Aldrich CC, Gulick AM. 2016 Structures of a nonribosomal peptide synthetase module bound to MbtH-like proteins support a highly dynamic domain architecture. J. Biol. Chem. 291, 22 559-22 571. (doi:10.1074/jbc.M116.746297) Crossref, Web of Science, Google Scholar
- 29. Kreitler DF, Gemmell EM, Schaffer JE, Wencewicz TA, Gulick AM. 2019 The structural basis of N-acyl-α-amino-β-lactone formation catalyzed by a nonribosomal peptide synthetase. Nat. Commun. 10, 3432. (doi:10.1038/s41467-019-11383-7) Crossref, PubMed, Web of Science, Google Scholar
- 30. Tanovic A, Samel SA, Essen L-O, Marahiel MA. 2008 Crystal structure of the termination module of a nonribosomal peptide synthetase. Science 321, 659-663. (doi:10.1126/science.1159850) Crossref, PubMed, Web of Science, Google Scholar
- 31. Gulick AM. 2009 Conformational dynamics in the Acyl-CoA synthetases, adenylation domains of non-ribosomal peptide synthetases, and firefly luciferase. ACS Chem. Biol. 4, 811-827. (doi:10.1021/cb900156h) Crossref, PubMed, Web of Science, Google Scholar
- 32. Mitchell CA, Shi C, Aldrich CC, Gulick AM. 2012 Structure of PA 1221, a nonribosomal peptide synthetase containing adenylation and peptidyl carrier protein domains. Biochemistry 51, 3252-3263. (doi:10.1021/bi300112e) Crossref, PubMed, Web of Science, Google Scholar
- 33. Branchini BR, Murtiashaw MH, Magyar RA, Anderson SM. 2000 The role of lysine 529, a conserved residue of the acyl-adenylate-forming enzyme superfamily, in firefly luciferase. Biochemistry 39, 5433-5440. (doi:10.1021/bi9928804) Crossref, PubMed, Web of Science, Google Scholar
- 34. Wu R, Reger AS, Lu X, Gulick AM, Dunaway-Mariano D. 2009 The mechanism of domain alternation in the acyl-adenylate forming ligase superfamily member 4-chlorobenzoate: coenzyme A ligase. Biochemistry 48, 4115-4125. (doi:10.1021/bi9002327) Crossref, PubMed, Web of Science, Google Scholar
- 35. Miller BR, Sundlov JA, Drake EJ, Makin TA, Gulick AM. 2014 Analysis of the linker region joining the adenylation and carrier protein domains of the modular nonribosomal peptide synthetases. Proteins 82, 2691-2702. (doi:10.1002/prot.24635) Crossref, PubMed, Web of Science, Google Scholar
- 36. Dowling DP, Kung Y, Croft AK, Taghizadeh K, Kelly WL, Walsh CT, Drennan CL. 2016 Structural elements of an NRPS cyclization domain and its intermodule docking domain. Proc. Natl Acad. Sci. USA 113, 12 432-12 437. (doi:10.1073/pnas.1608615113) Crossref, Web of Science, Google Scholar
- 37. Chen W-H, Li K, Guntaka NS, Bruner SD. 2016 Interdomain and intermodule organization in epimerization domain containing nonribosomal peptide synthetases. ACS Chem. Biol. 11, 2293-2303. (doi:10.1021/acschembio.6b00332) Crossref, PubMed, Web of Science, Google Scholar
- 38. Alonzo DA, Chiche-Lapierre C, Tarry MJ, Wang J, Schmeing TM. 2020 Structural basis of keto acid utilization in nonribosomal depsipeptide synthesis. Nat. Chem. Biol. 16, 493-496. (doi:10.1038/s41589-020-0481-5) Crossref, PubMed, Web of Science, Google Scholar
- 39. Mori S, Pang AH, Lundy TA, Garzan A, Tsodikov OV, Garneau-Tsodikova S. 2018 Structural basis for backbone N-methylation by an interrupted adenylation domain. Nat. Chem. Biol. 14, 428-430. (doi:10.1038/s41589-018-0014-7) Crossref, PubMed, Web of Science, Google Scholar
- 40. Pang B, Chen Y, Gan F, Yan C, Jin L, Gin JW, Petzold CJ, Keasling JD. 2020 Investigation of indigoidine synthetase reveals a conserved active-site base residue of nonribosomal peptide synthetase oxidases. J. Am. Chem. Soc. 142, 10 931-10 935. (doi:10.1021/jacs.0c04328) Crossref, Web of Science, Google Scholar
- 41. Labby KJ, Watsula SG, Garneau-Tsodikova S. 2015 Interrupted adenylation domains: unique bifunctional enzymes involved in nonribosomal peptide biosynthesis. Nat. Prod. Rep. 32, 641-653. (doi:10.1039/C4NP00120F) Crossref, PubMed, Web of Science, Google Scholar
- 42. Bloudoff K, Schmeing TM. 2017 Structural and functional aspects of the nonribosomal peptide synthetase condensation domain superfamily: discovery, dissection and diversity. Biochim. Biophys. Acta Proteins Proteom. 1865, 1587-1604. (doi:10.1016/j.bbapap.2017.05.010) Crossref, PubMed, Web of Science, Google Scholar
- 43. Smith HG, Beech MJ, Lewandowski JR, Challis GL, Jenner M. In press. Docking domain-mediated subunit interactions in natural product megasynth(et)ases. J. Ind. Microbiol. Biotechnol. Web of Science, Google Scholar
- 44. Dutta S 2014 Structure of a modular polyketide synthase. Nature 510, 512-517. (doi:10.1038/nature13423) Crossref, PubMed, Web of Science, Google Scholar
- 45. Whicher JR 2014 Structural rearrangements of a polyketide synthase module during its catalytic cycle. Nature 510, 560-564. (doi:10.1038/nature13409) Crossref, PubMed, Web of Science, Google Scholar
- 46. Shi C, Miller BR, Alexander EM, Gulick AM, Aldrich CC. 2020 Design, synthesis, and biophysical evaluation of mechanism-based probes for condensation domains of nonribosomal peptide synthetases. ACS Chem. Biol. 15, 1813-1819. (doi:10.1021/acschembio.0c00411) Crossref, PubMed, Web of Science, Google Scholar
- 47. Keating TA, Suo Z, Ehmann DE, Walsh CT. 2000 Selectivity of the yersiniabactin synthetase adenylation domain in the two-step process of amino acid activation and transfer to a holo-carrier protein domain. Biochemistry 39, 2297-2306. (doi:10.1021/bi992341z) Crossref, PubMed, Web of Science, Google Scholar
- 48. Ehmann DE, Shaw-Reid CA, Losey HC, Walsh CT. 2000 The EntF and EntE adenylation domains of Escherichia coli enterobactin synthetase: sequestration and selectivity in acyl-AMP transfers to thiolation domain cosubstrates. Proc. Natl Acad. Sci. USA 97, 2509-2514. (doi:10.1073/pnas.040572897) Crossref, PubMed, Web of Science, Google Scholar
- 49. Liu Y, Zheng T, Bruner SD. 2011 Structural basis for phosphopantetheinyl carrier domain interactions in the terminal module of nonribosomal peptide synthetases. Chem. Biol. 18, 1482-1488. (doi:10.1016/j.chembiol.2011.09.018) Crossref, PubMed, Google Scholar
- 50. Samel SA, Schoenafinger G, Knappe TA, Marahiel MA, Essen L-O. 2007 Structural and functional insights into a peptide bond-forming bidomain from a nonribosomal peptide synthetase. Structure 15, 781-792. (doi:10.1016/j.str.2007.05.008) Crossref, PubMed, Web of Science, Google Scholar
- 51. Marahiel MA. 2016 A structural model for multimodular NRPS assembly lines. Nat. Prod. Rep. 33, 136-140. (doi:10.1039/C5NP00082C) Crossref, PubMed, Web of Science, Google Scholar
- 52. Hoppert M, Gentzsch C, Schörgendorfer K. 2001 Structure and localization of cyclosporin synthetase, the key enzyme of cyclosporin biosynthesis in Tolypocladium inflatum. Arch. Microbiol. 176, 285-293. (doi:10.1007/s002030100324) Crossref, PubMed, Web of Science, Google Scholar
- 53. Tria G, Mertens HDT, Kachala M, Svergun DI. 2015 Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering. IUCrJ 2, 207-217. (doi:10.1107/S205225251500202X) Crossref, PubMed, Web of Science, Google Scholar
- 54. Kessler N, Schuhmann H, Morneweg S, Linne U, Marahiel MA. 2004 The linear pentadecapeptide gramicidin is assembled by four multimodular nonribosomal peptide synthetases that comprise 16 modules with 56 catalytic domains. J. Biol. Chem. 279, 7413-7419. (doi:10.1074/jbc.M309658200) Crossref, PubMed, Web of Science, Google Scholar
- 55. Shankar C, Veeraraghavan B, Nabarro LEB, Ravi R, Ragupathi NKD, Rupali P. 2018 Whole genome analysis of hypervirulent Klebsiella pneumoniae isolates from community and hospital acquired bloodstream infection. BMC Microbiol. 18, 6. (doi:10.1186/s12866-017-1148-6) Crossref, PubMed, Web of Science, Google Scholar
- 56. Peltier F, Choquet M, Decroix V, Adjidé CC, Castelain S, Guiheneuf R, Pluquet E. 2019 Characterization of a multidrug-resistant Klebsiella pneumoniae ST607-K25 clone responsible for a nosocomial outbreak in a neonatal intensive care unit. J. Med. Microbiol. 68, 67-76. (doi:10.1099/jmm.0.000884) Crossref, PubMed, Web of Science, Google Scholar
- 57. Remya PA, Shanthi M, Sekar U. 2019 Characterisation of virulence genes associated with pathogenicity in Klebsiella pneumoniae. Indian J. Med. Microbiol. 37, 210-218. (doi:10.4103/ijmm.IJMM_19_157) Crossref, PubMed, Web of Science, Google Scholar
- 58. Lawlor MS, O'connor C, Miller VL. 2007 Yersiniabactin is a virulence factor for Klebsiella pneumoniae during pulmonary infection. Infect. Immun. 75, 1463-1472. (doi:10.1128/IAI.00372-06) Crossref, PubMed, Web of Science, Google Scholar
- 59. Brown AS, Calcott MJ, Owen JG, Ackerley DF. 2018 Structural, functional and evolutionary perspectives on effective re-engineering of non-ribosomal peptide synthetase assembly lines. Nat. Prod. Rep. 35, 1210-1228. (doi:10.1039/C8NP00036K) Crossref, PubMed, Web of Science, Google Scholar
- 60. Bozhüyük KA, Micklefield J, Wilkinson B. 2019 Engineering enzymatic assembly lines to produce new antibiotics. Curr. Opin. Microbiol. 51, 88-96. (doi:10.1016/j.mib.2019.10.007) Crossref, PubMed, Web of Science, Google Scholar
- 61. Cane DE, Walsh CT, Khosla C. 1998 Harnessing the biosynthetic code: combinations, permutations, and mutations. Science 282, 63-68. (doi:10.1126/science.282.5386.63) Crossref, PubMed, Web of Science, Google Scholar
- 62. Kegler C, Bode HB. 2020 Artificial splitting of a non-ribosomal peptide synthetase by inserting natural docking domains. Angew. Chem. Int. Ed. Engl. 59, 13 463-13 467. (doi:10.1002/anie.201915989) Crossref, Web of Science, Google Scholar
- 63. Calcott MJ, Owen JG, Ackerley DF. 2020 Efficient rational modification of non-ribosomal peptides by adenylation domain substitution. Nat. Commun. 11, 4554. (doi:10.1038/s41467-020-18365-0) Crossref, PubMed, Web of Science, Google Scholar
- 64. Tietze A, Shi Y-N, Kronenwerth M, Bode HB. 2020 Nonribosomal peptides produced by minimal and engineered synthetases with terminal reductase domains. Chembiochem 21, 2750-2754. (doi:10.1002/cbic.202000176) Crossref, PubMed, Web of Science, Google Scholar
- 65. Ruijne F, Kuipers OP. 2021 Combinatorial biosynthesis for the generation of new-to-nature peptide antimicrobials. Biochem. Soc. Trans. 49, 203-215. (doi:10.1042/BST20200425) Crossref, PubMed, Web of Science, Google Scholar
- 66. Bozhüyük KAJ, Fleischhacker F, Linck A, Wesche F, Tietze A, Niesert C-P, Bode HB. 2018 De novo design and engineering of non-ribosomal peptide synthetases. Nat. Chem. 10, 275-281. (doi:10.1038/nchem.2890) Crossref, PubMed, Web of Science, Google Scholar
- 67. Bozhüyük KAJ 2019 Modification and de novo design of non-ribosomal peptide synthetases using specific assembly points within condensation domains. Nat. Chem. 11, 653-661. (doi:10.1038/s41557-019-0276-z) Crossref, PubMed, Web of Science, Google Scholar