New Insights into the Biosynthetic Logic of Ribosomally Synthesized and Post-translationally Modified Peptide Natural Products - PubMed (original) (raw)
Review
New Insights into the Biosynthetic Logic of Ribosomally Synthesized and Post-translationally Modified Peptide Natural Products
Manuel A Ortega et al. Cell Chem Biol. 2016.
Abstract
Ribosomally synthesized and post-translationally modified peptides (RiPPs) are a large group of structurally diverse natural products. Their biological activities and unique biosynthetic pathways have sparked a growing interest in RiPPs. Furthermore, the relatively low genetic complexity associated with RiPP biosynthesis makes them excellent candidates for synthetic biology applications. This Review highlights recent developments in the understanding of the biosynthesis of several bacterial RiPP family members, the use of the RiPP biosynthetic machinery for generating novel macrocyclic peptides, and the implementation of tools designed to guide the discovery and characterization of novel RiPPs.
Copyright © 2016 Elsevier Ltd. All rights reserved.
Figures
Figure 1
A window into RiPP biosynthesis. (A) Schematic RiPP biosynthetic pathway. Representative RiPP biosynthetic gene cluster where each gene encodes a biosynthetic enzyme color-coded by the modification it catalyzes. Dotted circles represent amino acids within the leader peptide. Full circles represent amino acids within the core region. (B) Chemical structures of select RiPP subfamily members. Structural features defining a particular RiPP subfamily are shown in blue. Additional PTMs are shown in red.
Figure 2
Overview of PTMs in lasso peptides, cyanobactins, and lanthipeptides. (A) Proposed biosynthetic scheme during the maturation of the lasso peptide microcin J25. Leader peptide is shown as dotted circles; core peptide is shown as a line. (B) PTMs often present in cyanobactins. (C) Proposed mechanism for the formation of azolines in cyanobactins catalyzed by YcaO-like cyclodehydratases. (D) Common PTMs found in lanthipeptides. (E–F) Proposed dehydration mechanism employed by (E) class I lanthipeptide dehydratases and (F) class II–IV lanthionine synthetases. (G) Proposed cyclization mechanism in lanthipeptides. Xn, connecting peptide.
Figure 3
Overview of PTMs in thiopeptides, sactipeptides, and streptide. (A) Putative macrocyclization mechanism involved in the generation of the characteristic central six-membered nitrogen-containing heterocycle in thiopeptides. To date no direct evidence has been provided favoring either a concerted or stepwise mechanism. (B) Proposed steps involved in the generation of MIA during nosiheptide biosynthesis catalyzed by NosL. (C) Trp methylation catalyzed by TsrM during thiostrepton biosynthesis. (D–E) Overview of SAM dependent transformations during (D) sactipeptide and (E) streptide biosynthesis. Xn, connecting peptide.
Figure 4
Leader peptide removal by RiPP PCATs. (A) General domain architecture of PCAT enzymes. (B) Proposed model of leader peptide removal with concomitant transport catalyzed by PCATs. (left) Cartoon representing the complex in its ATP-free (left) and ATP-bound (right) forms. Figure adapted from (Lin et al., 2015). TMD, transmembrane domain; NBD, nucleotide binding domain.
Figure 5
Recognition of the leader peptide by the RiPP biosynthetic machinery. (A–B) Cartoon (top) and surface (bottom) representation of the wHTH motif in (A) NisB in complex with NisA (PDB ID 4WD9), and (B) LynD in complex with PatE’ (PDB ID 4V1T). PatE’ and NisA leader peptide are shown in red (top) or green (bottom). (C–D) Cartoon representation of (C) PqqD (PDB ID 3G2B), and of (D) the putative leader peptide-binding site in CylM (PDB ID 5DZT). In all structures α helices are shown in cyan and β sheets are shown in magenta.
Figure 6
General strategy for RiPP genome mining and structural characterization. BGC, biosynthetic gene cluster.
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References
- Abts A, Montalban-Lopez M, Kuipers OP, Smits SH, Schmitt L. NisC binds the FxLx motif of the nisin leader peptide. Biochemistry. 2013;52:5387–95. - PubMed
- Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS, Bulaj G, Camarero JA, Campopiano DJ, Challis GL, Clardy J, et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep. 2013;30:108–60. - PMC - PubMed
- Beck-Sickinger AG, Jung G. Synthesis and conformational analysis of lantibiotic leader-, pro-, and pre-peptides. In: JUNG G, SAHL H-G, editors. Nisin and Novel Lantibiotics. Leiden: ESCOM; 1991.
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