New developments in RiPP discovery, enzymology and engineering

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

doi:10.1039/D0NP00027B

New developments in RiPP discovery, enzymology and engineering

Manuel Montalbán-López,

†^a Thomas A. Scott,

†^b Sangeetha Ramesh,

†^cd Imran R. Rahman,

†^e Auke J. van Heel,

†^f Jakob H. Viel,

†^f Vahe Bandarian,^g Elke Dittmann,

^h Olga Genilloud,

ⁱ Yuki Goto,

^j María José Grande Burgos,

^k Colin Hill,

^l Seokhee Kim,

^m Jesko Koehnke,

ⁿ John A. Latham,

^o A. James Link,

^p Beatriz Martínez,

^q Satish K. Nair,

^der Yvain Nicolet,

^s Sylvie Rebuffat,

^t Hans-Georg Sahl,^u Dipti Sareen,

^v Eric W. Schmidt,

^w Lutz Schmitt,

^x Konstantin Severinov,^y Roderich D. Süssmuth,

^z Andrew W. Truman,

^aa Huan Wang,

^ab Jing-Ke Weng,

^ac Gilles P. van Wezel,

^ad Qi Zhang,

^ae Jin Zhong,

^af Jörn Piel,

*^b Douglas A. Mitchell,

*^cdag Oscar P. Kuipers

*^f and Wilfred A. van der Donk

*^deagah

Author affiliations

* Corresponding authors

^a Department of Microbiology, University of Granada, Spain

^b Institute of Microbiology, ETH Zürich, Zürich, Switzerland
E-mail: jpiel@ethz.ch

^c Department of Microbiology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
E-mail: douglasm@illinois.edu

^d Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
E-mail: vddonk@illinois.edu

^e Department of Biochemistry, University of Illinois at Urbana-Champaign, Urbana, IL, USA

^f Dept. of Molecular Genetics, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, The Netherlands
E-mail: o.p.kuipers@rug.nl

^g Department of Chemistry, University of Utah, Salt Lake City, UT, USA

^h Institute of Biochemistry and Biology, University of Potsdam, Germany

ⁱ Fundación MEDINA, Granada, Spain

^j Department of Chemistry, Graduate School of Science, The University of Tokyo, Bunkyo, Tokyo, Japan

^k Department of Microbiology, University of Jaén, Spain

^l APC Microbiome Ireland, School of Microbiology, University College Cork, Cork, Ireland

^m Department of Chemistry, Seoul National University, South Korea

ⁿ School of Chemistry, University of Glasgow, Glasgow, UK

^o Department of Chemistry and Biochemistry, University of Denver, Denver, CO, USA

^p Departments of Chemical and Biological Engineering, Chemistry, and Molecular Biology, Princeton University, Princeton, NJ, USA

^q Dept. of Technology and Biotechnology of Dairy Products, Dairy Research Institute-IPLA, Consejo Superior de Investigaciones Científicas-CSIC, Villaviciosa, Spain

^r Center for Biophysics and Computational Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

^s Université Grenoble-Alpes, CEA, CNRS, IBS, Metalloproteins Unit, Grenoble, France

^t Laboratory Molecules of Communication and Adaptation of Microorganisms-MCAM (UMR 7245 CNRS-MNHN), National Museum of Natural History, Paris, France

^u Department of Pharmaceutical Microbiology, University of Bonn, Bonn, Germany

^v Department of Biochemistry, Panjab University, Chandigarh-160014, India

^w Department of Medicinal Chemistry, University of Utah, Salt Lake City, UT, USA

^x Institute of Biochemistry, Heinrich Heine University Düsseldorf, Duesseldorf, Germany

^y Waksman Institute, Rutgers University, Piscataway NJ and Skolkovo Institute of Science and Technology, Skolkovo, Russia

^z Department of Chemistry, Technische Universität Berlin, Berlin, Germany

^aa Department of Molecular Microbiology, John Innes Centre, Norwich, UK

^ab State Key Laboratory of Coordination Chemistry, Chemistry and Biomedicine Innovation Center of Nanjing University, School of Chemistry and Chemical Engineering, Nanjing University, Nanjing 210093, China

^ac Whitehead Institute for Biomedical Research, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA

^ad Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, The Netherlands

^ae Fudan University, Shanghai, China

^af State Key Laboratory of Microbial Resources, Institute of Microbiology, University of Chinese Academy of Sciences, Beijing, China

^ag Department of Chemistry, University of Illinois at Urbana-Champaign, Urbana, IL, USA

^ah Howard Hughes Medical Institute, University of Illinois at Urbana-Champaign, Urbana, IL, USA

Abstract

Covering: up to June 2020

Ribosomally-synthesized and post-translationally modified peptides (RiPPs) are a large group of natural products. A community-driven review in 2013 described the emerging commonalities in the biosynthesis of RiPPs and the opportunities they offered for bioengineering and genome mining. Since then, the field has seen tremendous advances in understanding of the mechanisms by which nature assembles these compounds, in engineering their biosynthetic machinery for a wide range of applications, and in the discovery of entirely new RiPP families using bioinformatic tools developed specifically for this compound class. The First International Conference on RiPPs was held in 2019, and the meeting participants assembled the current review describing new developments since 2013. The review discusses the new classes of RiPPs that have been discovered, the advances in our understanding of the installation of both primary and secondary post-translational modifications, and the mechanisms by which the enzymes recognize the leader peptides in their substrates. In addition, genome mining tools used for RiPP discovery are discussed as well as various strategies for RiPP engineering. An outlook section presents directions for future research.

Graphical abstract: New developments in RiPP discovery, enzymology and engineering

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New developments in RiPP discovery, enzymology and engineering

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