A Unique Tryptophan C-Prenyltransferase from the Kawaguchipeptin Biosynthetic Pathway

Overview

Journal Angew Chem Int Ed Engl

Specialty Chemistry

Date 2016 Feb 6

PMID 26846478

Citations 22

Authors

Anirudra Parajuli

Daniel H Kwak

Luca Dalponte

Niina Leikoski

Tomas Galica

Ugochukwu Umeobika

Laurent Trembleau

Andrew Bent

Kaarina Sivonen

Matti Wahlsten

Hao Wang

Ermanno Rizzi

Gianluca De Bellis

James Naismith

Marcel Jaspars

Xinyu Liu

Wael Houssen

David Peter Fewer

Affiliations

Soon will be listed here.

Abstract

Cyanobactins are a rapidly growing family of linear and cyclic peptides produced by cyanobacteria. Kawaguchipeptins A and B, two macrocyclic undecapeptides reported earlier from Microcystis aeruginosa NIES-88, are shown to be products of the cyanobactin biosynthetic pathway. The 9 kb kawaguchipeptin (kgp) gene cluster was identified in a 5.26 Mb draft genome of Microcystis aeruginosa NIES-88. We verified that this gene cluster is responsible for the production of the kawaguchipeptins through heterologous expression of the kgp gene cluster in Escherichia coli. The KgpF prenyltransferase was overexpressed and was shown to prenylate C-3 of Trp residues in both linear and cyclic peptides in vitro. Our findings serve to further enhance the structural diversity of cyanobactins to include tryptophan-prenylated cyclic peptides.

Citing Articles

Genome-informed Discovery of Monchicamides A-K: Cyanobactins from the Microcoleaceae Cyanobacterium LEGE 16532.

Castelo-Branco R, Pereira J, Freitas S, Preto M, Vieira A, Morais J J Nat Prod. 2024; 88(1):86-93.

PMID: 39718459 PMC: 11774001. DOI: 10.1021/acs.jnatprod.4c01063.

Cell-Free Systems: Ideal Platforms for Accelerating the Discovery and Production of Peptide-Based Antibiotics.

Park H, Jin H, Kim D, Lee J Int J Mol Sci. 2024; 25(16).

PMID: 39201795 PMC: 11354240. DOI: 10.3390/ijms25169109.

Genome Mining for New Enzyme Chemistry.

Nguyen D, Mitchell D, van der Donk W ACS Catal. 2024; 14(7):4536-4553.

PMID: 38601780 PMC: 11002830. DOI: 10.1021/acscatal.3c06322.

Chemoenzymatic Late-Stage Modifications Enable Downstream Click-Mediated Fluorescent Tagging of Peptides.

Colombano A, Dalponte L, DallAngelo S, Clemente C, Idress M, Ghazal A Angew Chem Int Ed Engl. 2023; 62(16):e202215979.

PMID: 36815722 PMC: 10946513. DOI: 10.1002/anie.202215979.

Emulating nonribosomal peptides with ribosomal biosynthetic strategies.

Mordhorst S, Ruijne F, Vagstad A, Kuipers O, Piel J RSC Chem Biol. 2023; 4(1):7-36.

PMID: 36685251 PMC: 9811515. DOI: 10.1039/d2cb00169a.

References

McIntosh J, Donia M, Nair S, Schmidt E . Enzymatic basis of ribosomal peptide prenylation in cyanobacteria. J Am Chem Soc. 2011; 133(34):13698-705. PMC: 3170831. DOI: 10.1021/ja205458h. View

Li S . Prenylated indole derivatives from fungi: structure diversity, biological activities, biosynthesis and chemoenzymatic synthesis. Nat Prod Rep. 2009; 27(1):57-78. DOI: 10.1039/b909987p. View

Magnuson R, Solomon J, Grossman A . Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell. 1994; 77(2):207-16. DOI: 10.1016/0092-8674(94)90313-1. View

Sivonen K, Leikoski N, Fewer D, Jokela J . Cyanobactins-ribosomal cyclic peptides produced by cyanobacteria. Appl Microbiol Biotechnol. 2010; 86(5):1213-25. PMC: 2854353. DOI: 10.1007/s00253-010-2482-x. View

Tsuji F, Kobayashi K, Okada M, Yamaguchi H, Ojika M, Sakagami Y . The geranyl-modified tryptophan residue is crucial for ComXRO-E-2 pheromone biological activity. Bioorg Med Chem Lett. 2011; 21(13):4041-4. DOI: 10.1016/j.bmcl.2011.04.123. View

Leikoski N, Fewer D, Sivonen K . Widespread occurrence and lateral transfer of the cyanobactin biosynthesis gene cluster in cyanobacteria. Appl Environ Microbiol. 2008; 75(3):853-7. PMC: 2632131. DOI: 10.1128/AEM.02134-08. View

Tatusov R, Fedorova N, Jackson J, Jacobs A, Kiryutin B, Koonin E . The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003; 4:41. PMC: 222959. DOI: 10.1186/1471-2105-4-41. View

Arnison P, Bibb M, Bierbaum G, Bowers A, Bugni T, Bulaj G . Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep. 2012; 30(1):108-60. PMC: 3954855. DOI: 10.1039/c2np20085f. View

Hulvova H, Galuszka P, Frebortova J, Frebort I . Parasitic fungus Claviceps as a source for biotechnological production of ergot alkaloids. Biotechnol Adv. 2012; 31(1):79-89. DOI: 10.1016/j.biotechadv.2012.01.005. View

10.

Lowe T, Eddy S . tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997; 25(5):955-64. PMC: 146525. DOI: 10.1093/nar/25.5.955. View

11.

Donia M, Ravel J, Schmidt E . A global assembly line for cyanobactins. Nat Chem Biol. 2008; 4(6):341-3. PMC: 2862271. DOI: 10.1038/nchembio.84. View

12.

Casey P, Seabra M . Protein prenyltransferases. J Biol Chem. 1996; 271(10):5289-92. DOI: 10.1074/jbc.271.10.5289. View

13.

Lee J, McIntosh J, Hathaway B, Schmidt E . Using marine natural products to discover a protease that catalyzes peptide macrocyclization of diverse substrates. J Am Chem Soc. 2009; 131(6):2122-4. PMC: 2645028. DOI: 10.1021/ja8092168. View

14.

McIntosh J, Donia M, Schmidt E . Ribosomal peptide natural products: bridging the ribosomal and nonribosomal worlds. Nat Prod Rep. 2009; 26(4):537-59. PMC: 2975598. DOI: 10.1039/b714132g. View

15.

Shanks R, Kadouri D, MacEachran D, OToole G . New yeast recombineering tools for bacteria. Plasmid. 2009; 62(2):88-97. PMC: 2737453. DOI: 10.1016/j.plasmid.2009.05.002. View

16.

McIntosh J, Lin Z, Tianero M, Schmidt E . Aestuaramides, a natural library of cyanobactin cyclic peptides resulting from isoprene-derived Claisen rearrangements. ACS Chem Biol. 2013; 8(5):877-83. PMC: 3657307. DOI: 10.1021/cb300614c. View

17.

Delcher A, Bratke K, Powers E, Salzberg S . Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007; 23(6):673-9. PMC: 2387122. DOI: 10.1093/bioinformatics/btm009. View

18.

Wallwey C, Li S . Ergot alkaloids: structure diversity, biosynthetic gene clusters and functional proof of biosynthetic genes. Nat Prod Rep. 2010; 28(3):496-510. DOI: 10.1039/c0np00060d. View

19.

Gibbs J, Oliff A . The potential of farnesyltransferase inhibitors as cancer chemotherapeutics. Annu Rev Pharmacol Toxicol. 1997; 37:143-66. DOI: 10.1146/annurev.pharmtox.37.1.143. View

20.

Donia M, Schmidt E . Linking chemistry and genetics in the growing cyanobactin natural products family. Chem Biol. 2011; 18(4):508-19. PMC: 3119926. DOI: 10.1016/j.chembiol.2011.01.019. View