Nonribosomal Peptide Synthesis Definitely Working Out of the Rules
Abstract
1. Introduction
2. Canonical Rules for Nonribosomal Synthesis
2.1. Modular Assembly Lines including Core Domains
2.2. Secondary Domains
2.3. Modes of Biosynthesis
3. Domains Working Out of the Canonical Rules
3.1. C Domains Working Differently
3.2. Discovery of New Rare Secondary Domains
3.3. Secondary Domains Nested within A Domains
3.4. Domains Ending an Assembly Line
4. Amazing Modes of Biosynthesis
4.1. How to Overcome the Lack of Functional A or C Domains
4.2. Complex Nonlinear Modes of Biosynthesis
5. Conclusions/Outcomes
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Süssmuth, R.D.; Mainz, A. Nonribosomal Peptide Synthesis—Principles and Prospects. Angew. Chem. 2017, 56, 3770–3821. [Google Scholar] [CrossRef] [PubMed]
- Dell, M.; Dunbar, K.L.; Hertweck, C. Ribosome-independent peptide biosynthesis: The challenge of a unifying nomenclature. Nat. Prod. Rep. 2022. [Google Scholar] [CrossRef]
- Reva, O.; Tümmler, B. Think big–giant genes in bacteria. Environ. Microbiol. 2008, 10, 768–777. [Google Scholar] [CrossRef] [PubMed]
- Weissman, K.J. The structural biology of biosynthetic megaenzymes. Nat. Chem. Biol. 2015, 11, 660–670. [Google Scholar] [CrossRef]
- Esmaeel, Q.; Pupin, M.; Jacques, P.; Leclère, V. Nonribosomal peptides and polyketides of Burkholderia: New compounds potentially implicated in biocontrol and pharmaceuticals. Environ. Sci. Pollut. Res. 2018, 25, 29794–29807. [Google Scholar] [CrossRef] [PubMed]
- Blin, K.; Shaw, S.; Kloosterman, A.M.; Charlop-Powers, Z.; Van Wezel, G.P.; Medema, M.H.; Weber, T. AntiSMASH 6.0: Improving cluster detection and comparison capabilities. Nucleic Acids Res. 2021, 49, W29–W35. [Google Scholar] [CrossRef] [PubMed]
- Pupin, M.; Esmaeel, Q.; Flissi, A.; Dufresne, Y.; Jacques, P.; Leclère, V. Norine: A powerful resource for novel nonribosomal peptide discovery. Synth. Syst. Biotechnol. 2016, 1, 89–94. [Google Scholar] [CrossRef]
- Pupin, M.; Flissi, A.; Jacques, P.; Leclère, V. Bioinformatics tools for the discovery of new lipopeptides with biocontrol applications. Eur. J. Plant Pathol. 2018, 152, 993–1001. [Google Scholar] [CrossRef]
- Chevrette, M.G.; Aicheler, F.; Kohlbacher, O.; Currie, C.R.; Medema, M.H. SANDPUMA: Ensemble predictions of nonribosomal peptide chemistry reveal biosynthetic diversity across Actinobacteria. Bioinformatics 2017, 33, 3202–3210. [Google Scholar] [CrossRef] [PubMed]
- Liangcheng, D.; Shen, B. Identification and characterization of a type II peptidyl carrier protein from the bleomycin producer Streptomyces verticillus ATCC 15003. Chem. Biol. 1999, 6, 507–517. [Google Scholar] [CrossRef]
- Sieber, S.A.; Marahiel, M.A. Molecular mechanisms underlying nonribosomal peptide synthesis: Approaches to new antibiotics. Chem. Rev. 2005, 105, 715–738. [Google Scholar] [CrossRef] [PubMed]
- Marahiel, M.A. A structural model for multimodular NRPS assembly lines. Nat. Prod. Rep. 2016, 33, 136–140. [Google Scholar] [CrossRef]
- Dehling, E.; Rüschenbaum, J.; Diecker, J.; Dörner, W.; Mootz, H.D. Photo-crosslink analysis in nonribosomal peptide synthetases reveals aberrant gel migration of branched crosslink isomers and spatial proximity between non-neighboring domains. Chem. Sci. 2020, 11, 8945–8954. [Google Scholar] [CrossRef]
- Hahn, M.; Stachelhaus, T. Selective interaction between nonribosomal peptide synthetases is facilitated by short communication-mediating domains. Proc. Natl. Acad. Sci. USA 2004, 101, 15585–15590. [Google Scholar] [CrossRef] [PubMed]
- Chiocchini, C.; Linne, U.; Stachelhaus, T. In Vivo Biocombinatorial Synthesis of Lipopeptides by COM Domain-Mediated Reprogramming of the Surfactin Biosynthetic Complex. Chem. Biol. 2006, 13, 899–908. [Google Scholar] [CrossRef]
- Fage, C.D.; Kosol, S.; Jenner, M.; Öster, C.; Gallo, A.; Kaniusaite, M.; Steinbach, R.; Staniforth, M.; Stavros, V.G.; Marahiel, M.A.; et al. Communication Breakdown: Dissecting the COM Interfaces between the Subunits of Nonribosomal Peptide Synthetases. ACS Catal. 2021, 11, 10802–10813. [Google Scholar] [CrossRef]
- Caboche, S.; Leclère, V.; Pupin, M.; Kucherov, G.; Jacques, P. Diversity of monomers in nonribosomal peptides: Towards the prediction of origin and biological activity. J. Bacteriol. 2010, 192, 5143–5150. [Google Scholar] [CrossRef] [PubMed]
- Flissi, A.; Ricart, E.; Campart, C.; Chevalier, M.; Dufresne, Y.; Michalik, J.; Jacques, P.; Flahaut, C.; Lisacek, F.; Leclère, V.; et al. Norine: Update of the nonribosomal peptide resource. Nucleic Acids Res. 2019, 48, D465–D469. [Google Scholar] [CrossRef]
- Marahiel, M.A.; Stachelhaus, T.; Mootz, H.D. Modular Peptide Synthetases Involved in Nonribosomal Peptide Synthesis. Chem. Rev. 1997, 97, 2651–2674. [Google Scholar] [CrossRef] [PubMed]
- Conti, E.; Stachelhaus, T.; Marahiel, M.A.; Brick, P. Structural basis for the activation of phenylalanine in the non-ribosomal biosynthesis of gramicidin S. EMBO J. 1997, 16, 4174–4183. [Google Scholar] [CrossRef] [PubMed]
- Challis, G.L.; Ravel, J.; Townsend, C.A. Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem. Biol. 2000, 7, 211–224. [Google Scholar] [CrossRef]
- Scaglione, A.; Fullone, M.R.; Montemiglio, L.C.; Parisi, G.; Zamparelli, C.; Vallone, B.; Savino, C.; Grgurina, I. Structure of the adenylation domain Thr1 involved in the biosynthesis of 4-chlorothreonine in Streptomyces sp. OH-5093-protein flexibility and molecular bases of substrate specificity. FEBS J. 2017, 284, 2981–2999. [Google Scholar] [CrossRef] [PubMed]
- Stachelhaus, T.; Mootz, H.D.; Marahiel, M.A. The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol. 1999, 6, 493–505. [Google Scholar] [CrossRef]
- Rausch, C.; Weber, T.; Kohlbacher, O.; Wohlleben, W.; Huson, D.H. Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res. 2005, 33, 5799–5808. [Google Scholar] [CrossRef] [PubMed]
- Röttig, M.; Medema, M.H.; Blin, K.; Weber, T.; Rausch, C.; Kohlbacher, O. NRPSpredictor2-A web server for predicting NRPS adenylation domain specificity. Nucleic Acids Res. 2011, 39, W362–W367. [Google Scholar] [CrossRef]
- Esmaeel, Q.; Chevalier, M.; Chataigné, G.; Subashkumar, R.; Jacques, P.; Leclère, V. Nonribosomal peptide synthetase with a unique iterative-alternative-optional mechanism catalyzes amonabactin synthesis in Aeromonas. Appl. Microbiol. Biotechnol. 2016, 100, 8453–8463. [Google Scholar] [CrossRef]
- Ma, Z.; Geudens, N.; Kieu, N.P.; Sinnaeve, D.; Ongena, M.; Martins, J.C.; Höfte, M. Biosynthesis, chemical structure, and structure-activity relationship of orfamide lipopeptides produced by Pseudomonas protegens and related species. Front. Microbiol. 2016, 7, 382. [Google Scholar] [CrossRef]
- Girard, L.; Höfte, M.; Mot, R. De Lipopeptide families at the interface between pathogenic and beneficial Pseudomonas-plant interactions. Crit. Rev. Microbiol. 2020, 46, 397–419. [Google Scholar] [CrossRef]
- Théatre, A.; Cano-Prieto, C.; Bartolini, M.; Laurin, Y.; Deleu, M.; Niehren, J.; Fida, T.; Gerbinet, S.; Alanjary, M.; Medema, M.H.; et al. The Surfactin-Like Lipopeptides from Bacillus spp.: Natural Biodiversity and Synthetic Biology for a Broader Application Range. Front. Bioeng. Biotechnol. 2021, 9, 623701. [Google Scholar] [CrossRef]
- Huang, T.; Duan, Y.; Zou, Y.; Deng, Z.; Lin, S. NRPS Protein MarQ Catalyzes Flexible Adenylation and Specific S-Methylation. ACS Chem. Biol. 2018, 13, 2387–2391. [Google Scholar] [CrossRef]
- De Roo, V.; Verleysen, Y.; Kovács, B.; De Vleeschouwer, M.; Girard, L.; Höfte, M.; De Mot, R.; Madder, A.; Geudens, N.; Martins, J.C. An NMR fingerprint matching approach for the identification and structural re-evaluation of Pseudomonas lipopeptides. bioRxiv 2022. [Google Scholar] [CrossRef]
- Izoré, T.; Cryle, M.J. The many faces and important roles of protein-protein interactions during non-ribosomal peptide synthesis. Nat. Prod. Rep. 2018, 35, 1120–1139. [Google Scholar] [CrossRef] [PubMed]
- Winn, M.; Fyans, J.K.; Zhuo, Y.; Micklefield, J. Recent advances in engineering nonribosomal peptide assembly lines. Nat. Prod. Rep. 2016, 33, 317–347. [Google Scholar] [CrossRef] [PubMed]
- Rausch, C.; Hoof, I.; Weber, T.; Wohlleben, W.; Huson, D.H. Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution. BMC Evol. Biol. 2007, 7, 1–15. [Google Scholar] [CrossRef]
- Ziemert, N.; Podell, S.; Penn, K.; Badger, J.H.; Allen, E.; Jensen, P.R. The Natural Product Domain Seeker NaPDoS: A Phylogeny Based Bioinformatic Tool to Classify Secondary Metabolite Gene Diversity. PLoS ONE 2012, 7, e34064. [Google Scholar] [CrossRef] [PubMed]
- Kaniusaite, M.; Tailhades, J.; Marschall, E.A.; Goode, R.J.A.; Schittenhelm, R.B.; Cryle, M.J. A proof-reading mechanism for non-proteinogenic amino acid incorporation into glycopeptide antibiotics. Chem. Sci. 2019, 10, 9466–9482. [Google Scholar] [CrossRef] [PubMed]
- Izoré, T.; Candace Ho, Y.T.; Kaczmarski, J.A.; Gavriilidou, A.; Chow, K.H.; Steer, D.L.; Goode, R.J.A.; Schittenhelm, R.B.; Tailhades, J.; Tosin, M.; et al. Structures of a non-ribosomal peptide synthetase condensation domain suggest the basis of substrate selectivity. Nat. Commun. 2021, 12, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Tahlan, K.; Moore, M.A.; Jensen, S.E. δ-(l-α-aminoadipyl)-l-cysteinyl-d-valine synthetase (ACVS): Discovery and perspectives. J. Ind. Microbiol. Biotechnol. 2017, 44, 517–524. [Google Scholar] [CrossRef]
- Cane, D.E.; Walsh, C.T. The parallel and convergent universes of polyketide synthases and nonribosomal peptide synthetases. Chem. Biol. 1999, 6, 319–325. [Google Scholar] [CrossRef]
- Marahiel, M.A. Working outside the protein-synthesis rules: Insights into non-ribosomal peptide synthesis. J. Pept. Sci. 2009, 15, 799–807. [Google Scholar] [CrossRef]
- Kries, H. Biosynthetic engineering of nonribosomal peptide synthetases. J. Pept. Sci. 2016, 22, 564–570. [Google Scholar] [CrossRef] [PubMed]
- Labby, K.J.; Watsula, S.G.; Garneau-Tsodikova, S. Interrupted adenylation domains: Unique bifunctional enzymes involved in nonribosomal peptide biosynthesis. Nat. Prod. Rep. 2015, 32, 641–653. [Google Scholar] [CrossRef] [PubMed]
- Booth, T.J.; Bozhüyük, K.A.J.; Liston, J.D.; Lacey, E.; Wilkinson, B. Bifurcation drives the evolution of assembly-line biosynthesis. bioRxiv 2021. [Google Scholar] [CrossRef]
- Hur, G.H.; Vickery, C.R.; Burkart, M.D. Explorations of catalytic domains in non-ribosomal peptide synthetase enzymology. Nat. Prod. Rep. 2012, 29, 1074–1098. [Google Scholar] [CrossRef] [PubMed]
- McErlean, M.; Overbay, J.; Van Lanen, S. Refining and expanding nonribosomal peptide synthetase function and mechanism. J. Ind. Microbiol. Biotechnol. 2019, 46, 493–513. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.; Feng, P.; Yin, Y.; Bushley, K.; Spatafora, J.W.; Wang, C. Cyclosporine biosynthesis in Tolypocladium inflatum benefits fungal adaptation to the environment. mBio 2018, 9, e01211–e01218. [Google Scholar] [CrossRef]
- Ansari, M.Z.; Sharma, J.; Gokhale, R.S.; Mohanty, D. In silico analysis of methyltransferase domains involved in biosynthesis of secondary metabolites. BMC Bioinform. 2008, 9, 1–21. [Google Scholar] [CrossRef] [PubMed]
- Gao, X.; Haynes, S.W.; Ames, B.D.; Wang, P.; Vien, L.P.; Walsh, C.T.; Tang, Y. Cyclization of fungal nonribosomal peptides by a terminal condensation-like domain. Nat. Chem. Biol. 2012, 8, 823–830. [Google Scholar] [CrossRef] [PubMed]
- Velkov, T.; Horne, J.; Scanlon, M.J.; Capuano, B.; Yuriev, E.; Lawen, A. Characterization of the N-methyltransferase activities of the multifunctional polypeptide cyclosporin synthetase. Chem. Biol. 2011, 18, 464–475. [Google Scholar] [CrossRef] [PubMed]
- Rouhiainen, L.; Paulin, L.; Suomalainen, S.; Hyytiäinen, H.; Buikema, W.; Haselkorn, R.; Sivonen, K. Genes encoding synthetases of cyclic depsipeptides, anabaenopeptilides, in Anabaena strain 90. Mol. Microbiol. 2000, 37, 156–167. [Google Scholar] [CrossRef] [PubMed]
- Kessler, N.; Schuhmann, H.; Morneweg, S.; Linne, U.; Marahiel, M.A. The Linear Pentadecapeptide Gramicidin Is Assembled by Four Multimodular Nonribosomal Peptide Synthetases That Comprise 16 Modules with 56 Catalytic Domains. J. Biol. Chem. 2004, 279, 7413–7419. [Google Scholar] [CrossRef] [PubMed]
- Bode, H.B.; Brachmann, A.O.; Jadhav, K.B.; Seyfarth, L.; Dauth, C.; Fuchs, S.W.; Kaiser, M.; Waterfield, N.R.; Sack, H.; Heinemann, S.H.; et al. Structure Elucidation and Activity of KolossinA, the D-/L-Pentadecapeptide Product of a Giant Nonribosomal Peptide Synthetase. Angew. Chem. 2015, 54, 10352–10355. [Google Scholar] [CrossRef] [PubMed]
- Esmaeel, Q.; Pupin, M.; Kieu, N.P.; Chataigné, G.; Béchet, M.; Deravel, J.; Krier, F.; Höfte, M.; Jacques, P.; Leclère, V. Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. Microbiol. Open 2016, 5, 512–526. [Google Scholar] [CrossRef]
- Kenjić, N.; Hoag, M.R.; Moraski, G.C.; Caperelli, C.A.; Moran, G.R.; Lamb, A.L. PvdF of pyoverdin biosynthesis is a structurally unique N 10 -formyltetrahydrofolate-dependent formyltransferase. Arch. Biochem. Biophys. 2019, 664, 40–50. [Google Scholar] [CrossRef] [PubMed]
- Mootz, H.D.; Schwarzer, D.; Marahiel, M.A. Ways of assembling complex natural products on modular nonribosomal peptide synthetases. ChemBioChem 2002, 3, 490–504. [Google Scholar] [CrossRef]
- Ongena, M.; Jacques, P. Bacillus lipopeptides: Versatile weapons for plant disease biocontrol. Trends Microbiol. 2008, 16, 115–125. [Google Scholar] [CrossRef]
- Geudens, N.; Martins, J.C. Cyclic lipodepsipeptides from Pseudomonas spp.-Biological Swiss-Army knives. Front. Microbiol. 2018, 9, 1867. [Google Scholar] [CrossRef]
- Little, R.F.; Hertweck, C. Correction: Chain release mechanisms in polyketide and non-ribosomal peptide biosynthesis. Nat. Prod. Rep. 2022, 39, 206–207. [Google Scholar] [CrossRef] [PubMed]
- Reitz, Z.L.; Sandy, M.; Butler, A. Biosynthetic considerations of triscatechol siderophores framed on serine and threonine macrolactone scaffolds. Metallomics 2017, 9, 824–839. [Google Scholar] [CrossRef] [PubMed]
- Magarvey, N.A.; Haltli, B.; He, M.; Greenstein, M.; Hucul, J.A. Biosynthetic pathway for mannopeptimycins, lipoglycopeptide antibiotics active against drug-resistant gram-positive pathogens. Antimicrob. Agents Chemother. 2006, 50, 2167–2177. [Google Scholar] [CrossRef] [PubMed]
- Balibar, C.J.; Vaillancourt, F.H.; Walsh, C.T. Generation of D amino acid residues in assembly of arthrofactin by dual condensation/epimerization domains. Chem. Biol. 2005, 12, 1189–1200. [Google Scholar] [CrossRef]
- Dashti, Y.; Nakou, I.T.; Mullins, A.J.; Webster, G.; Jian, X.; Mahenthiralingam, E.; Challis, G.L. Discovery and Biosynthesis of Bolagladins: Unusual Lipodepsipeptides from Burkholderia gladioli Clinical Isolates. Angew. Chem. 2020, 59, 21553–21561. [Google Scholar] [CrossRef] [PubMed]
- Royer, M.; Koebnik, R.; Marguerettaz, M.; Barbe, V.; Robin, G.P.; Brin, C.; Carrere, S.; Gomez, C.; Hügelland, M.; Völler, G.H.; et al. Genome mining reveals the genus Xanthomonas to be a promising reservoir for new bioactive non-ribosomally synthesized peptides. BMC Genom. 2013, 14, 1–19. [Google Scholar] [CrossRef] [PubMed]
- Bloudoff, K.; Schmeing, T.M. Structural and functional aspects of the nonribosomal peptide synthetase condensation domain superfamily: Discovery, dissection and diversity. Biochim. Biophys. Acta Proteins Proteom. 2017, 1865, 1587–1604. [Google Scholar] [CrossRef]
- Duerfahrt, T.; Eppelmann, K.; Mülller, R.; Marahiel, M.A. Rational Design of a Bimodular Model System for the Investigation of Heterocyclization in Nonribosomal Peptide Biosynthesis Thomas. Chem. Biol. 2004, 11, 261–271. [Google Scholar] [CrossRef][Green Version]
- Gaudelli, N.M.; Townsend, C.A. Epimerization and substrate gating by a TE domain in β-lactam antibiotic biosynthesis. Nat. Chem. Biol. 2014, 10, 251–258. [Google Scholar] [CrossRef] [PubMed]
- Raaijmakers, J.M.; de Bruijn, I.; Nybroe, O.; Ongena, M. Natural functions of lipopeptides from Bacillus and Pseudomonas: More than surfactants and antibiotics. FEMS Microbiol. Rev. 2010, 34, 1037–1062. [Google Scholar] [CrossRef] [PubMed]
- Duitman, E.H.; Hamoen, L.W.; Rembold, M.; Venema, G.; Seitz, H.; Saenger, W.; Bernhard, F.; Reinhardt, R.; Schmidt, M.; Ullrich, C.; et al. The mycosubtilin synthetase of Bacillus subtilis ATCC6633: A multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase. Proc. Natl. Acad. Sci. USA 1999, 96, 13294–13299. [Google Scholar] [CrossRef]
- Tsuge, K.; Akiyama, T.; Shoda, M. Cloning, sequencing, and characterization of the iturin A operon. J. Bacteriol. 2001, 183, 6265–6273. [Google Scholar] [CrossRef]
- Luo, C.; Liu, X.; Zhou, H.; Wang, X.; Chen, Z. Nonribosomal peptide synthase gene clusters for lipopeptide biosynthesis in Bacillus subtilis 916 and their phenotypic functions. Appl. Environ. Microbiol. 2015, 81, 422–431. [Google Scholar] [CrossRef] [PubMed]
- Baltz, R. Biosynthesis and Genetic Engineering of Lipopeptide Antibiotics Related to Daptomycin. Curr. Top. Med. Chem. 2008, 8, 618–638. [Google Scholar] [CrossRef]
- Haslinger, K.; Peschke, M.; Brieke, C.; Maximowitsch, E.; Cryle, M.J. X-domain of peptide synthetases recruits oxygenases crucial for glycopeptide biosynthesis. Nature 2015, 521, 105–109. [Google Scholar] [CrossRef] [PubMed]
- Yim, G.; Thaker, M.N.; Koteva, K.; Wright, G. Glycopeptide antibiotic biosynthesis. J. Antibiot. 2014, 67, 31–41. [Google Scholar] [CrossRef]
- Peschke, M.; Brieke, C.; Cryle, M.J. F-O-G Ring Formation in Glycopeptide Antibiotic Biosynthesis is Catalysed by OxyE. Sci. Rep. 2016, 6, 1–9. [Google Scholar] [CrossRef]
- Peschke, M.; Gonsior, M.; Süssmuth, R.D.; Cryle, M.J. Understanding the crucial interactions between Cytochrome P450s and non-ribosomal peptide synthetases during glycopeptide antibiotic biosynthesis. Curr. Opin. Struct. Biol. 2016, 41, 46–53. [Google Scholar] [CrossRef] [PubMed]
- Peschke, M.; Brieke, C.; Heimes, M.; Cryle, M.J. The Thioesterase Domain in Glycopeptide Antibiotic Biosynthesis Is Selective for Cross-Linked Aglycones. ACS Chem. Biol. 2018, 13, 110–120. [Google Scholar] [CrossRef] [PubMed]
- Rosconi, F.; Davyt, D.; Martínez, V.; Martínez, M.; Abin-Carriquiry, J.A.; Zane, H.; Butler, A.; de Souza, E.M.; Fabiano, E. Identification and structural characterization of serobactins, a suite of lipopeptide siderophores produced by the grass endophyte Herbaspirillum seropedicae. Environ. Microbiol. 2013, 15, 916–927. [Google Scholar] [CrossRef] [PubMed]
- Kem, M.P.; Butler, A. Acyl peptidic siderophores: Structures, biosyntheses and post-assembly modifications. BioMetals 2015, 28, 445–459. [Google Scholar] [CrossRef]
- Singh, G.M.; Fortin, P.D.; Koglin, A.; Walsh, C.T. β-hydroxylation of the aspartyl residue in the phytotoxin syringomycin E: Characterization of two candidate hydroxylases AspH and SyrP in Pseudomonas syringae. Biochemistry 2008, 47, 11310–11320. [Google Scholar] [CrossRef]
- Hardy, C.D.; Butler, A. β-Hydroxyaspartic acid in siderophores: Biosynthesis and reactivity. J. Biol. Inorg. Chem. 2018, 23, 957–967. [Google Scholar] [CrossRef]
- Koonin, E.V.; Tatusove, R.L. Computer analysis of bacterial haloacid dehalogenases defines a large superfamily of hydrolases with diverse specificity. Application of an iterative approach to database search. J. Mol. Biol. 1994, 244, 125–132. [Google Scholar] [CrossRef] [PubMed]
- Etzbach, L.; Plaza, A.; Garcia, R.; Baumann, S.; Müller, R. Cystomanamides: Structure and biosynthetic pathway of a family of glycosylated lipopeptides from myxobacteria. Org. Lett. 2014, 16, 2414–2417. [Google Scholar] [CrossRef] [PubMed]
- Auerbach, D.; Yan, F.; Zhang, Y.; Müller, R. Characterization of an Unusual Glycerate Esterification Process in Vioprolide Biosynthesis. ACS Chem. Biol. 2018, 13, 3123–3130. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Oliver, R.A.; Townsend, C.A. Identification and Characterization of the Sulfazecin Monobactam Biosynthetic Gene Cluster. Cell Chem. Biol. 2017, 24, 24–34. [Google Scholar] [CrossRef] [PubMed]
- Desriac, F.; Jégou, C.; Balnois, E.; Brillet, B.; Le Chevalier, P.; Fleury, Y. Antimicrobial peptides from marine proteobacteria. Mar. Drugs 2013, 11, 3632–3660. [Google Scholar] [CrossRef] [PubMed]
- Murcia, N.R.; Lee, X.; Waridel, P.; Maspoli, A.; Imker, H.J.; Chai, T.; Walsh, C.T.; Reimmann, C. The Pseudomonas aeruginosa antimetabolite L -2-amino-4-methoxy-trans-3-butenoic acid (AMB) is made from glutamate and two alanine residues via a thiotemplate-linked tripeptide precursor. Front. Microbiol. 2015, 6, 170. [Google Scholar] [CrossRef]
- Gulick, A.M. Nonribosomal peptide synthetase biosynthetic clusters of ESKAPE pathogens. Nat. Prod. Rep. 2017, 34, 981–1009. [Google Scholar] [CrossRef]
- Patteson, J.B.; Dunn, Z.D.; Li, B. In Vitro Biosynthesis of the Nonproteinogenic Amino Acid Methoxyvinylglycine. Angew. Chem. 2018, 57, 6780–6785. [Google Scholar] [CrossRef]
- Mori, S.; Pang, A.H.; Lundy, T.A.; Garzan, A.; Tsodikov, O.V.; Garneau-Tsodikova, S. Structural basis for backbone N-methylation by an interrupted adenylation domain. Nat. Chem. Biol. 2018, 14, 428–430. [Google Scholar] [CrossRef]
- Walsh, C.T.; Wencewicz, T.A. Flavoenzymes: Versatile catalysts in biosynthetic pathways. Nat. Prod. Rep. 2013, 30, 175–200. [Google Scholar] [CrossRef]
- Kotowska, M.; Pawlik, K. Roles of type II thioesterases and their application for secondary metabolite yield improvement. Appl. Microbiol. Biotechnol. 2014, 98, 7735–7746. [Google Scholar] [CrossRef]
- Hou, J.; Robbel, L.; Marahiel, M.A. Identification and characterization of the lysobactin biosynthetic gene cluster reveals mechanistic insights into an unusual termination module architecture. Chem. Biol. 2011, 18, 655–664. [Google Scholar] [CrossRef]
- Mandalapu, D.; Ji, X.; Chen, J.; Guo, C.; Liu, W.Q.; Ding, W.; Zhou, J.; Zhang, Q. Thioesterase-Mediated Synthesis of Teixobactin Analogues: Mechanism and Substrate Specificity. J. Org. Chem. 2018, 83, 7271–7275. [Google Scholar] [CrossRef] [PubMed]
- Götze, S.; Stallforth, P. Structure, properties, and biological functions of nonribosomal lipopeptides from pseudomonads. Nat. Prod. Rep. 2020, 37, 29–54. [Google Scholar] [CrossRef] [PubMed]
- D’aes, J.; Kieu, N.P.; Léclère, V.; Tokarski, C.; Olorunleke, F.E.; De Maeyer, K.; Jacques, P.; Höfte, M.; Ongena, M.; Leclère, V.; et al. To settle or to move? The interplay between two classes of cyclic lipopeptides in the biocontrol strain Pseudomonas CMR12a. Environ. Microbiol. 2014, 16, 2282–2300. [Google Scholar] [CrossRef]
- Gross, H.; Loper, J.E. Genomics of secondary metabolite production by Pseudomonas spp. Nat. Prod. Rep. 2009, 26, 1408–1446. [Google Scholar] [CrossRef] [PubMed]
- De Bruijn, I.; De Kock, M.J.D.; Yang, M.; De Waard, P.; Van Beek, T.A.; Raaijmakers, J.M. Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol. Microbiol. 2007, 63, 417–428. [Google Scholar] [CrossRef] [PubMed]
- Caradec, T.; Pupin, M.; Vanvlassenbroeck, A.; Devignes, M.D.; Smaïl-Tabbone, M.; Jacques, P.; Leclère, V. Prediction of monomer isomery in florine: A workflow dedicated to nonribosomal peptide discovery. PLoS ONE 2014, 9, e85667. [Google Scholar] [CrossRef]
- Schafhauser, T.; Kirchner, N.; Kulik, A.; Huijbers, M.M.E.; Flor, L.; Caradec, T.; Fewer, D.P.; Gross, H.; Jacques, P.; Jahn, L.; et al. The cyclochlorotine mycotoxin is produced by the nonribosomal peptide synthetase CctN in Talaromyces islandicus (‘Penicillium islandicum’). Environ. Microbiol. 2016, 18, 3728–3741. [Google Scholar] [CrossRef]
- Du, L.; Lou, L. PKS and NRPS release mechanisms. Nat. Prod. Rep. 2010, 27, 255–278. [Google Scholar] [CrossRef]
- Deshpande, S.; Altermann, E.; Sarojini, V.; Lott, J.S.; Lee, T.V. Structural characterization of a PCP–R didomain from an archaeal nonribosomal peptide synthetase reveals novel interdomain interactions. J. Biol. Chem. 2021, 296, 100432. [Google Scholar] [CrossRef]
- Li, L.; Deng, W.; Song, J.; Ding, W.; Zhao, Q.F.; Peng, C.; Song, W.W.; Tang, G.L.; Liu, W. Characterization of the saframycin a gene cluster from Streptomyces lavendulae NRRL 11002 revealing a nonribosomal peptide synthetase system for assembling the unusual tetrapeptidyl skeleton in an iterative manner. J. Bacteriol. 2008, 190, 251–263. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; McClure, R.A.; Zheng, Y.; Thomson, R.J.; Kelleher, N.L. Proteomics guided discovery of flavopeptins: Anti-proliferative aldehydes synthesized by a reductase domain-containing non-ribosomal peptide synthetase. J. Am. Chem. Soc. 2013, 135, 10449–10456. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Weissman, K.J.; Müller, R. Myxochelin biosynthesis: Direct evidence for two- and four-electron reduction of a carrier protein-bound thioester. J. Am. Chem. Soc. 2008, 130, 7554–7555. [Google Scholar] [CrossRef] [PubMed]
- Barajas, J.F.; Phelan, R.M.; Schaub, A.J.; Kliewer, J.T.; Kelly, P.J.; Jackson, D.R.; Luo, R.; Keasling, J.D.; Tsai, S.C. Comprehensive Structural and Biochemical Analysis of the Terminal Myxalamid Reductase Domain for the Engineered Production of Primary Alcohols. Chem. Biol. 2015, 22, 1018–1029. [Google Scholar] [CrossRef]
- Schracke, N.; Linne, U.; Mahlert, C.; Marahiel, M.A. Synthesis of linear gramicidin requires the cooperation of two independent reductases. Biochemistry 2005, 44, 8507–8513. [Google Scholar] [CrossRef] [PubMed]
- Wyatt, M.A.; Mok, M.C.Y.; Junop, M.; Magarvey, N.A. Heterologous Expression and Structural Characterisation of a Pyrazinone Natural Product Assembly Line. ChemBioChem 2012, 13, 2408–2415. [Google Scholar] [CrossRef] [PubMed]
- Kopp, F.; Mahlert, C.; Grünewald, J.; Marahiel, M.A. Peptide macrocyclization: The reductase of the nostocyclopeptide synthetase triggers the self-assembly of a macrocyclic imine. J. Am. Chem. Soc. 2006, 128, 16478–16479. [Google Scholar] [CrossRef]
- Li, Z.; de Vries, R.H.; Chakraborty, P.; Song, C.; Zhao, X.; Scheffers, D.J.; Roelfes, G.; Kuipers, O.P. Novel Modifications of Nonribosomal Peptides from Brevibacillus laterosporus MG64 and Investigation of Their Mode of Action. Appl. Environ. Microbiol. 2020, 86, 1–14. [Google Scholar] [CrossRef]
- Sims, J.W.; Schmidt, E.W. Thioesterase-like role for fungal PKS-NRPS hybrid reductive domains. J. Am. Chem. Soc. 2008, 130, 11149–11155. [Google Scholar] [CrossRef]
- Eley, K.L.; Halo, L.M.; Song, Z.; Powles, H.; Cox, R.J.; Bailey, A.M.; Lazarus, C.M.; Simpson, T.J. Biosynthesis of the 2-pyridone tenellin in the insect pathogenic fungus Beauveria bassiana. ChemBioChem 2007, 8, 289–297. [Google Scholar] [CrossRef] [PubMed]
- Cociancich, S.; Pesic, A.; Petras, D.; Uhlmann, S.; Kretz, J.; Schubert, V.; Vieweg, L.; Duplan, S.; Marguerettaz, M.; Noëll, J.; et al. The gyrase inhibitor albicidin consists of p-aminobenzoic acids and cyanoalanine. Nat. Chem. Biol. 2015, 11, 195–197. [Google Scholar] [CrossRef] [PubMed]
- Baumann, S.; Herrmann, J.; Raju, R.; Steinmetz, H.; Mohr, K.I.; Hüttel, S.; Harmrolfs, K.; Stadler, M.; Müller, R. Cystobactamids: Myxobacterial topoisomerase inhibitors exhibiting potent antibacterial activity. Angew. Chem. 2014, 53, 14605–14609. [Google Scholar] [CrossRef] [PubMed]
- Groß, S.; Schnell, B.; Haack, P.A.; Auerbach, D.; Müller, R. In vivo and in vitro reconstitution of unique key steps in cystobactamid antibiotic biosynthesis. Nat. Commun. 2021, 12, 1–15. [Google Scholar] [CrossRef] [PubMed]
- McCafferty, D.G.; Cudic, P.; Frankel, B.A.; Barkallah, S.; Kruger, R.G.; Li, W. Chemistry and biology of the ramoplanin family of peptide antibiotics. Pept. Sci. 2002, 66, 261–284. [Google Scholar] [CrossRef] [PubMed]
- Yin, X.; Zabriskie, T.M. The enduracidin biosynthetic gene cluster from Streptomyces fungicidicus. Microbiology 2006, 152, 2969–2983. [Google Scholar] [CrossRef] [PubMed]
- Pu, J.Y.; Peng, C.; Tang, M.C.; Zhang, Y.; Guo, J.P.; Song, L.Q.; Hua, Q.; Tang, G.L. Naphthyridinomycin biosynthesis revealing the use of leader peptide to guide nonribosomal peptide assembly. Org. Lett. 2013, 15, 3674–3677. [Google Scholar] [CrossRef] [PubMed]
- Pan, H.X.; Li, J.A.; Shao, L.; Zhu, C.B.; Chen, J.S.; Tang, G.L.; Chen, D.J. Genetic manipulation revealing an unusual N-terminal region in a stand-alone non-ribosomal peptide synthetase involved in the biosynthesis of ramoplanins. Biotechnol. Lett. 2013, 35, 107–114. [Google Scholar] [CrossRef] [PubMed]
- Jenner, M.; Jian, X.; Dashti, Y.; Masschelein, J.; Hobson, C.; Roberts, D.M.; Jones, C.; Harris, S.; Parkhill, J.; Raja, H.A.; et al. An unusual: Burkholderia gladioli double chain-initiating nonribosomal peptide synthetase assembles “fungal” icosalide antibiotics. Chem. Sci. 2019, 10, 5489–5494. [Google Scholar] [CrossRef] [PubMed]
- Dose, B.; Niehs, S.P.; Scherlach, K.; Flórez, L.V.; Kaltenpoth, M.; Hertweck, C. Unexpected Bacterial Origin of the Antibiotic Icosalide: Two-Tailed Depsipeptide Assembly in Multifarious Burkholderia Symbionts. ACS Chem. Biol. 2018, 13, 2414–2420. [Google Scholar] [CrossRef] [PubMed]
- Hamano, Y. Occurrence, biosynthesis, biodegradation, and industrial and medical applications of a naturally occurringε-Poly-L-lysine. Biosci. Biotechnol. Biochem. 2011, 75, 1226–1233. [Google Scholar] [CrossRef]
- Kito, N.; Maruyama, C.; Yamanaka, K.; Imokawa, Y.; Utagawa, T.; Hamano, Y. Mutational analysis of the three tandem domains of ε-poly-l-lysine synthetase catalyzing the l-lysine polymerization reaction. J. Biosci. Bioeng. 2013, 115, 523–526. [Google Scholar] [CrossRef] [PubMed]
- Jiang, X.; Radko, Y.; Gren, T.; Palazzotto, E.; Jørgensen, T.S.; Cheng, T.; Xian, M.; Weber, T.; Lee, S.Y. Distribution of ε-Poly-L-Lysine Synthetases in Coryneform Bacteria Isolated from Cheese and Human Skin. Appl. Environ. Microbiol. 2021, 87, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Hermes, C.; Richarz, R.; Wirtz, D.A.; Patt, J.; Hanke, W.; Kehraus, S.; Voß, J.H.; Küppers, J.; Ohbayashi, T.; Namasivayam, V.; et al. Thioesterase-mediated side chain transesterification generates potent Gq signaling inhibitor FR900359. Nat. Commun. 2021, 12, 144. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Duban, M.; Cociancich, S.; Leclère, V. Nonribosomal Peptide Synthesis Definitely Working Out of the Rules. Microorganisms 2022, 10, 577. https://doi.org/10.3390/microorganisms10030577
Duban M, Cociancich S, Leclère V. Nonribosomal Peptide Synthesis Definitely Working Out of the Rules. Microorganisms. 2022; 10(3):577. https://doi.org/10.3390/microorganisms10030577
Chicago/Turabian StyleDuban, Matthieu, Stéphane Cociancich, and Valérie Leclère. 2022. "Nonribosomal Peptide Synthesis Definitely Working Out of the Rules" Microorganisms 10, no. 3: 577. https://doi.org/10.3390/microorganisms10030577
APA StyleDuban, M., Cociancich, S., & Leclère, V. (2022). Nonribosomal Peptide Synthesis Definitely Working Out of the Rules. Microorganisms, 10(3), 577. https://doi.org/10.3390/microorganisms10030577