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Article

Heterologous Production of β-Caryophyllene and Evaluation of Its Activity against Plant Pathogenic Fungi

by
Fabienne Hilgers
1,†,
Samer S. Habash
2,†,
Anita Loeschcke
1,
Yannic Sebastian Ackermann
1,
Stefan Neumann
2,
Achim Heck
3,
Oliver Klaus
1,
Jennifer Hage-Hülsmann
1,
Florian M. W. Grundler
2,
Karl-Erich Jaeger
1,3,
A. Sylvia S. Schleker
2,* and
Thomas Drepper
1,*
1
Institute of Molecular Enzyme Technology, Heinrich-Heine-University Düsseldorf, Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich, Germany
2
INRES—Molecular Phytomedicine, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115 Bonn, Germany
3
Institute of Bio- and Geosciences (IBG-1: Biotechnology) Forschungszentrum Jülich, Wilhelm-Johnen-Straße, 52428 Jülich, Germany
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Microorganisms 2021, 9(1), 168; https://doi.org/10.3390/microorganisms9010168
Submission received: 10 December 2020 / Revised: 8 January 2021 / Accepted: 10 January 2021 / Published: 14 January 2021
(This article belongs to the Special Issue Microbial Secondary Metabolites and Biotechnology)

Abstract

Terpenoids constitute one of the largest and most diverse groups within the class of secondary metabolites, comprising over 80,000 compounds. They not only exhibit important functions in plant physiology but also have commercial potential in the biotechnological, pharmaceutical, and agricultural sectors due to their promising properties, including various bioactivities against pathogens, inflammations, and cancer. In this work, we therefore aimed to implement the plant sesquiterpenoid pathway leading to β-caryophyllene in the heterologous host Rhodobacter capsulatus and achieved a maximum production of 139 ± 31 mg L−1 culture. As this sesquiterpene offers various beneficial anti-phytopathogenic activities, we evaluated the bioactivity of β-caryophyllene and its oxygenated derivative β-caryophyllene oxide against different phytopathogenic fungi. Here, both compounds significantly inhibited the growth of Sclerotinia sclerotiorum and Fusarium oxysporum by up to 40%, while growth of Alternaria brassicicola was only slightly affected, and Phoma lingam and Rhizoctonia solani were unaffected. At the same time, the compounds showed a promising low inhibitory profile for a variety of plant growth-promoting bacteria at suitable compound concentrations. Our observations thus give a first indication that β-caryophyllene and β-caryophyllene oxide are promising natural agents, which might be applicable for the management of certain plant pathogenic fungi in agricultural crop production.
Keywords: terpenoids; sesquiterpene production; Rhodobacter capsulatus; β-caryophyllene; bioactivity; phytopathogens; plant pathogenic fungi; plant growth-promoting bacteria terpenoids; sesquiterpene production; Rhodobacter capsulatus; β-caryophyllene; bioactivity; phytopathogens; plant pathogenic fungi; plant growth-promoting bacteria
Graphical Abstract

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MDPI and ACS Style

Hilgers, F.; Habash, S.S.; Loeschcke, A.; Ackermann, Y.S.; Neumann, S.; Heck, A.; Klaus, O.; Hage-Hülsmann, J.; Grundler, F.M.W.; Jaeger, K.-E.; et al. Heterologous Production of β-Caryophyllene and Evaluation of Its Activity against Plant Pathogenic Fungi. Microorganisms 2021, 9, 168. https://doi.org/10.3390/microorganisms9010168

AMA Style

Hilgers F, Habash SS, Loeschcke A, Ackermann YS, Neumann S, Heck A, Klaus O, Hage-Hülsmann J, Grundler FMW, Jaeger K-E, et al. Heterologous Production of β-Caryophyllene and Evaluation of Its Activity against Plant Pathogenic Fungi. Microorganisms. 2021; 9(1):168. https://doi.org/10.3390/microorganisms9010168

Chicago/Turabian Style

Hilgers, Fabienne, Samer S. Habash, Anita Loeschcke, Yannic Sebastian Ackermann, Stefan Neumann, Achim Heck, Oliver Klaus, Jennifer Hage-Hülsmann, Florian M. W. Grundler, Karl-Erich Jaeger, and et al. 2021. "Heterologous Production of β-Caryophyllene and Evaluation of Its Activity against Plant Pathogenic Fungi" Microorganisms 9, no. 1: 168. https://doi.org/10.3390/microorganisms9010168

APA Style

Hilgers, F., Habash, S. S., Loeschcke, A., Ackermann, Y. S., Neumann, S., Heck, A., Klaus, O., Hage-Hülsmann, J., Grundler, F. M. W., Jaeger, K.-E., Schleker, A. S. S., & Drepper, T. (2021). Heterologous Production of β-Caryophyllene and Evaluation of Its Activity against Plant Pathogenic Fungi. Microorganisms, 9(1), 168. https://doi.org/10.3390/microorganisms9010168

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