N-Prenylation of Tryptophan by an Aromatic Prenyltransferase from the Cyanobactin Biosynthetic Pathway
- Luca Dalponte
Luca DalponteMarine Biodiscovery Centre, Department of Chemistry, University of Aberdeen, Meston Walk, Aberdeen AB24 3UE, U.K.Institute of Medical Sciences, University of Aberdeen, Ashgrove Road West, Aberdeen AB25 2ZD, U.K.More by Luca Dalponte
- ,
- Anirudra Parajuli
Anirudra ParajuliDepartment of Microbiology, University of Helsinki, Viikki Biocenter 1, Viikinkaari 9, 00014 Helsinki, FinlandMore by Anirudra Parajuli
- ,
- Ellen Younger
Ellen YoungerMarine Biodiscovery Centre, Department of Chemistry, University of Aberdeen, Meston Walk, Aberdeen AB24 3UE, U.K.Institute of Medical Sciences, University of Aberdeen, Ashgrove Road West, Aberdeen AB25 2ZD, U.K.More by Ellen Younger
- ,
- Antti Mattila
Antti MattilaDepartment of Microbiology, University of Helsinki, Viikki Biocenter 1, Viikinkaari 9, 00014 Helsinki, FinlandMore by Antti Mattila
- ,
- Jouni Jokela
Jouni JokelaDepartment of Microbiology, University of Helsinki, Viikki Biocenter 1, Viikinkaari 9, 00014 Helsinki, FinlandMore by Jouni Jokela
- ,
- Matti Wahlsten
Matti WahlstenDepartment of Microbiology, University of Helsinki, Viikki Biocenter 1, Viikinkaari 9, 00014 Helsinki, FinlandMore by Matti Wahlsten
- ,
- Niina Leikoski
Niina LeikoskiDepartment of Microbiology, University of Helsinki, Viikki Biocenter 1, Viikinkaari 9, 00014 Helsinki, FinlandMore by Niina Leikoski
- ,
- Kaarina Sivonen
Kaarina SivonenDepartment of Microbiology, University of Helsinki, Viikki Biocenter 1, Viikinkaari 9, 00014 Helsinki, FinlandMore by Kaarina Sivonen
- ,
- Scott A. Jarmusch
Scott A. JarmuschMarine Biodiscovery Centre, Department of Chemistry, University of Aberdeen, Meston Walk, Aberdeen AB24 3UE, U.K.More by Scott A. Jarmusch
- ,
- Wael E. Houssen*
Wael E. Houssen*E-mail: [email protected]Marine Biodiscovery Centre, Department of Chemistry, University of Aberdeen, Meston Walk, Aberdeen AB24 3UE, U.K.Institute of Medical Sciences, University of Aberdeen, Ashgrove Road West, Aberdeen AB25 2ZD, U.K.Pharmacognosy Department, Faculty of Pharmacy, Mansoura University, Mansoura 35516, EgyptMore by Wael E. Houssen
- , and
- David P. Fewer*
David P. Fewer*E-mail: [email protected]Department of Microbiology, University of Helsinki, Viikki Biocenter 1, Viikinkaari 9, 00014 Helsinki, FinlandMore by David P. Fewer
Abstract
Aromatic prenylation is an important step in the biosynthesis of many natural products and leads to an astonishing diversity of chemical structures. Cyanobactin pathways frequently encode aromatic prenyltransferases that catalyze the prenylation of these macrocyclic and linear peptides. Here we characterized the anacyclamide (acy) biosynthetic gene cluster from Anabaena sp. UHCC-0232. Partial reconstitution of the anacyclamide pathway, heterologous expression, and in vitro biochemical characterization demonstrate that the AcyF enzyme, encoded in the acy biosynthetic gene cluster, is a Trp N-prenyltransferase. Bioinformatic analysis suggests the monophyletic origin and rapid diversification of cyanobactin prenyltransferase enzymes and the multiple origins of N-1 Trp prenylation in prenylated natural products. The AcyF enzyme displayed high flexibility toward a range of Trp-containing substrates and represents an interesting new tool for biocatalytic applications.
Cited By
This article is cited by 25 publications.
- Yuchen Zhang, Keisuke Hamada, Masayuki Satake, Toru Sengoku, Yuki Goto, Hiroaki Suga. Switching Prenyl Donor Specificities of Cyanobactin Prenyltransferases. Journal of the American Chemical Society 2023, 145 (44) , 23893-23898. https://doi.org/10.1021/jacs.3c07373
- Yiwu Zheng, Ying Cong, Eric W. Schmidt, Satish K. Nair. Catalysts for the Enzymatic Lipidation of Peptides. Accounts of Chemical Research 2022, 55 (9) , 1313-1323. https://doi.org/10.1021/acs.accounts.2c00108
- PalfeyBruce A.Associate Professor, Biological Chemistry & Associate Director, Program in Chemical Biologybrupalf@umich.
edu SwitzerRebecca L.Assistant Professor of Chemistryrebecca.switzer@bucknell. Rumin Zhang, VP, Head of Biochemistry, Volastra Therapeutics, Lauren Parr, PhD Candidate, Department of Chemistry, University of Iowa. Kinetics of Enzyme Catalysis. 2022https://doi.org/10.1021/acsinfocus.7e5015edu - Chin-Soon Phan, Kenichi Matsuda, Nandani Balloo, Kei Fujita, Toshiyuki Wakimoto, Tatsufumi Okino. Argicyclamides A–C Unveil Enzymatic Basis for Guanidine Bis-prenylation. Journal of the American Chemical Society 2021, 143 (27) , 10083-10087. https://doi.org/10.1021/jacs.1c05732
- Antti Mattila, Rose-Marie Andsten, Mikael Jumppanen, Michele Assante, Jouni Jokela, Matti Wahlsten, Kornelia M. Mikula, Cihad Sigindere, Daniel H. Kwak, Muriel Gugger, Harri Koskela, Kaarina Sivonen, Xinyu Liu, Jari Yli-Kauhaluoma, Hideo Iwaï, David P. Fewer. Biosynthesis of the Bis-Prenylated Alkaloids Muscoride A and B. ACS Chemical Biology 2019, 14 (12) , 2683-2690. https://doi.org/10.1021/acschembio.9b00620
- Yuchen Zhang, Yuki Goto, Hiroaki Suga. Modulating the Acceptor Preference of His‐C‐Geranyltransferase LimF. Israel Journal of Chemistry 2024, https://doi.org/10.1002/ijch.202300182
- Azusa Miyata, Sohei Ito, Daisuke Fujinami. Structure Prediction and Genome Mining‐Aided Discovery of the Bacterial C‐Terminal Tryptophan Prenyltransferase PalQ. Advanced Science 2024, 11 (6) https://doi.org/10.1002/advs.202307372
- Xiaodan Ouyang, Paul M. D'Agostino, Matti Wahlsten, Endrews Delbaje, Jouni Jokela, Perttu Permi, Greta Gaiani, Antti Poso, Piia Bartos, Tobias A. M. Gulder, Hannu Koistinen, David P. Fewer. Direct pathway cloning and expression of the radiosumin biosynthetic gene cluster. Organic & Biomolecular Chemistry 2023, 21 (23) , 4893-4908. https://doi.org/10.1039/D3OB00385J
- Yuxin Fu, Yanli Xu, Fleur Ruijne, Oscar P Kuipers. Engineering lanthipeptides by introducing a large variety of RiPP modifications to obtain new-to-nature bioactive peptides. FEMS Microbiology Reviews 2023, 47 (3) https://doi.org/10.1093/femsre/fuad017
- Alessandro Colombano, Luca Dalponte, Sergio Dall'Angelo, Claudia Clemente, Mohannad Idress, Ahmad Ghazal, Wael E. Houssen. Chemoenzymatic Late‐Stage Modifications Enable Downstream Click‐Mediated Fluorescent Tagging of Peptides. Angewandte Chemie International Edition 2023, 62 (16) https://doi.org/10.1002/anie.202215979
- Alessandro Colombano, Luca Dalponte, Sergio Dall'Angelo, Claudia Clemente, Mohannad Idress, Ahmad Ghazal, Wael E. Houssen. Chemoenzymatic Late‐Stage Modifications Enable Downstream Click‐Mediated Fluorescent Tagging of Peptides. Angewandte Chemie 2023, 135 (16) https://doi.org/10.1002/ange.202215979
- Yuchen Zhang, Yuki Goto, Hiroaki Suga. Discovery, biochemical characterization, and bioengineering of cyanobactin prenyltransferases. Trends in Biochemical Sciences 2023, 48 (4) , 360-374. https://doi.org/10.1016/j.tibs.2022.11.002
- Silja Mordhorst, Fleur Ruijne, Anna L. Vagstad, Oscar P. Kuipers, Jörn Piel. Emulating nonribosomal peptides with ribosomal biosynthetic strategies. RSC Chemical Biology 2023, 4 (1) , 7-36. https://doi.org/10.1039/D2CB00169A
- Claudia Clemente, Nicholas Johnson, Xiaodan Ouyang, Rafael V. Popin, Sergio Dall'Angelo, Matti Wahlsten, Jouni Jokela, Alessandro Colombano, Brunello Nardone, David P. Fewer, Wael E. Houssen. Biochemical characterization of a cyanobactin arginine- N -prenylase from the autumnalamide biosynthetic pathway. Chemical Communications 2022, 58 (86) , 12054-12057. https://doi.org/10.1039/D2CC01799G
- Yuchen Zhang, Keisuke Hamada, Dinh Thanh Nguyen, Sumika Inoue, Masayuki Satake, Shunsuke Kobayashi, Chikako Okada, Kazuhiro Ogata, Masahiro Okada, Toru Sengoku, Yuki Goto, Hiroaki Suga. LimF is a versatile prenyltransferase for histidine-C-geranylation on diverse non-natural substrates. Nature Catalysis 2022, 5 (8) , 682-693. https://doi.org/10.1038/s41929-022-00822-2
- Mugilarasi Purushothaman, Snigdha Sarkar, Maho Morita, Muriel Gugger, Eric W. Schmidt, Brandon I. Morinaka. Genome‐Mining‐Based Discovery of the Cyclic Peptide Tolypamide and TolF, a Ser/Thr Forward O ‐Prenyltransferase. Angewandte Chemie 2021, 133 (15) , 8541-8546. https://doi.org/10.1002/ange.202015975
- Mugilarasi Purushothaman, Snigdha Sarkar, Maho Morita, Muriel Gugger, Eric W. Schmidt, Brandon I. Morinaka. Genome‐Mining‐Based Discovery of the Cyclic Peptide Tolypamide and TolF, a Ser/Thr Forward O ‐Prenyltransferase. Angewandte Chemie International Edition 2021, 60 (15) , 8460-8465. https://doi.org/10.1002/anie.202015975
- Tung Le, Wilfred A. van der Donk. Mechanisms and Evolution of Diversity-Generating RiPP Biosynthesis. Trends in Chemistry 2021, 3 (4) , 266-278. https://doi.org/10.1016/j.trechm.2021.01.003
- Manuel Montalbán-López, Thomas A. Scott, Sangeetha Ramesh, Imran R. Rahman, Auke J. van Heel, Jakob H. Viel, Vahe Bandarian, Elke Dittmann, Olga Genilloud, Yuki Goto, María José Grande Burgos, Colin Hill, Seokhee Kim, Jesko Koehnke, John A. Latham, A. James Link, Beatriz Martínez, Satish K. Nair, Yvain Nicolet, Sylvie Rebuffat, Hans-Georg Sahl, Dipti Sareen, Eric W. Schmidt, Lutz Schmitt, Konstantin Severinov, Roderich D. Süssmuth, Andrew W. Truman, Huan Wang, Jing-Ke Weng, Gilles P. van Wezel, Qi Zhang, Jin Zhong, Jörn Piel, Douglas A. Mitchell, Oscar P. Kuipers, Wilfred A. van der Donk. New developments in RiPP discovery, enzymology and engineering. Natural Product Reports 2021, 38 (1) , 130-239. https://doi.org/10.1039/D0NP00027B
- Rui Liu, Hongchi Zhang, Weiqiang Wu, Hui Li, Zhipeng An, Feng Zhou. C7-Prenylation of Tryptophan-Containing Cyclic Dipeptides by 7-Dimethylallyl Tryptophan Synthase Significantly Increases the Anticancer and Antimicrobial Activities. Molecules 2020, 25 (16) , 3676. https://doi.org/10.3390/molecules25163676
- Takahiro Mori. Enzymatic studies on aromatic prenyltransferases. Journal of Natural Medicines 2020, 74 (3) , 501-512. https://doi.org/10.1007/s11418-020-01393-x
- Bryce P. Johnson, Erin M. Scull, Dustin A. Dimas, Tejaswi Bavineni, Chandrasekhar Bandari, Andrea L. Batchev, Eric D. Gardner, Susan L. Nimmo, Shanteri Singh. Acceptor substrate determines donor specificity of an aromatic prenyltransferase: expanding the biocatalytic potential of NphB. Applied Microbiology and Biotechnology 2020, 104 (10) , 4383-4395. https://doi.org/10.1007/s00253-020-10529-8
- David P. Fewer, Mikko Metsä‐Ketelä. A pharmaceutical model for the molecular evolution of microbial natural products. The FEBS Journal 2020, 287 (7) , 1429-1449. https://doi.org/10.1111/febs.15129
- Camila M. Crnkovic, Jana Braesel, Aleksej Krunic, Alessandra S. Eustáquio, Jimmy Orjala. Scytodecamide from the Cultured Scytonema sp. UIC 10036 Expands the Chemical and Genetic Diversity of Cyanobactins. ChemBioChem 2020, 21 (6) , 845-852. https://doi.org/10.1002/cbic.201900511
- Wael E. Houssen. Peptide Cyclization Catalyzed by Cyanobactin Macrocyclases. 2019, 193-210. https://doi.org/10.1007/978-1-4939-9546-2_11