Larvae of the Clothing Moth <i>Tineola bisselliella</i> Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin

The evolutionary success of insects is promoted by their association with beneficial microbes that enable the utilization of unusual diets. The synanthropic clothing moth <i>Tineola bisselliella</i> provides an intriguing example of this phenomenon. The caterpillars of this species have...

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Main Authors: Andreas Vilcinskas, Michael Schwabe, Karina Brinkrolf, Rudy Plarre, Natalie Wielsch, Heiko Vogel
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/9/1415
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author Andreas Vilcinskas
Michael Schwabe
Karina Brinkrolf
Rudy Plarre
Natalie Wielsch
Heiko Vogel
author_facet Andreas Vilcinskas
Michael Schwabe
Karina Brinkrolf
Rudy Plarre
Natalie Wielsch
Heiko Vogel
author_sort Andreas Vilcinskas
collection DOAJ
description The evolutionary success of insects is promoted by their association with beneficial microbes that enable the utilization of unusual diets. The synanthropic clothing moth <i>Tineola bisselliella</i> provides an intriguing example of this phenomenon. The caterpillars of this species have adapted to feed on keratin-rich diets such as feathers and wool, which cannot be digested by most other animals and are resistant to common digestive enzymes. Inspired by the hypothesis that this ability may be conferred by symbiotic microbes, we utilized a simple assay to detect keratinase activity and a method to screen gut bacteria for candidate enzymes, which were isolated from feather-fed larvae. The isolation of DNA from keratin-degrading bacterial strains followed by de novo genome sequencing resulted in the identification of a novel bacterial strain related to <i>Bacillus</i> sp. FDAARGOS_235. Genome annotation identified 20 genes with keratinase domains. Proteomic analysis of the culture supernatant from this gut bacterium grown in non-nutrient buffer supplemented with feathers revealed several candidate enzymes potentially responsible for keratin degradation, including a thiol-disulfide oxidoreductase and multiple proteases. Our results suggest that the unusual diet of <i>T. bisselliella</i> larvae promotes their association with keratinolytic microorganisms and that the ability of larvae to feed on keratin can at least partially be attributed to bacteria that produce a cocktail of keratin-degrading enzymes.
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spelling doaj.art-4554f166728e45fe95a0c5d4ed8c03a32023-11-20T13:42:12ZengMDPI AGMicroorganisms2076-26072020-09-0189141510.3390/microorganisms8091415Larvae of the Clothing Moth <i>Tineola bisselliella</i> Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of KeratinAndreas Vilcinskas0Michael Schwabe1Karina Brinkrolf2Rudy Plarre3Natalie Wielsch4Heiko Vogel5Institute for Insect Biotechnology, Justus-Liebig-University of Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, GermanyDepartment of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Giessen, GermanyDepartment of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Giessen, GermanyBiologische Materialschädigung und Referenzorganismen, Bundesanstalt für Materialforschung und -prüfung (BAM), Unter den Eichen 87, 12205 Berlin, GermanyResearch Group Mass Spectrometry/Proteomics, Max-Planck Institute for Chemical Ecology, Hans-Knoell-Strasse 8, 07745 Jena, GermanyEntomology Department, Max-Planck Institute for Chemical Ecology, Hans-Knoell-Strasse 8, 07745 Jena, GermanyThe evolutionary success of insects is promoted by their association with beneficial microbes that enable the utilization of unusual diets. The synanthropic clothing moth <i>Tineola bisselliella</i> provides an intriguing example of this phenomenon. The caterpillars of this species have adapted to feed on keratin-rich diets such as feathers and wool, which cannot be digested by most other animals and are resistant to common digestive enzymes. Inspired by the hypothesis that this ability may be conferred by symbiotic microbes, we utilized a simple assay to detect keratinase activity and a method to screen gut bacteria for candidate enzymes, which were isolated from feather-fed larvae. The isolation of DNA from keratin-degrading bacterial strains followed by de novo genome sequencing resulted in the identification of a novel bacterial strain related to <i>Bacillus</i> sp. FDAARGOS_235. Genome annotation identified 20 genes with keratinase domains. Proteomic analysis of the culture supernatant from this gut bacterium grown in non-nutrient buffer supplemented with feathers revealed several candidate enzymes potentially responsible for keratin degradation, including a thiol-disulfide oxidoreductase and multiple proteases. Our results suggest that the unusual diet of <i>T. bisselliella</i> larvae promotes their association with keratinolytic microorganisms and that the ability of larvae to feed on keratin can at least partially be attributed to bacteria that produce a cocktail of keratin-degrading enzymes.https://www.mdpi.com/2076-2607/8/9/1415insect biotechnologybeneficial microbessymbiosiskeratindietary adaptationTineola bisselliella
spellingShingle Andreas Vilcinskas
Michael Schwabe
Karina Brinkrolf
Rudy Plarre
Natalie Wielsch
Heiko Vogel
Larvae of the Clothing Moth <i>Tineola bisselliella</i> Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin
Microorganisms
insect biotechnology
beneficial microbes
symbiosis
keratin
dietary adaptation
Tineola bisselliella
title Larvae of the Clothing Moth <i>Tineola bisselliella</i> Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin
title_full Larvae of the Clothing Moth <i>Tineola bisselliella</i> Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin
title_fullStr Larvae of the Clothing Moth <i>Tineola bisselliella</i> Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin
title_full_unstemmed Larvae of the Clothing Moth <i>Tineola bisselliella</i> Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin
title_short Larvae of the Clothing Moth <i>Tineola bisselliella</i> Maintain Gut Bacteria that Secrete Enzyme Cocktails to Facilitate the Digestion of Keratin
title_sort larvae of the clothing moth i tineola bisselliella i maintain gut bacteria that secrete enzyme cocktails to facilitate the digestion of keratin
topic insect biotechnology
beneficial microbes
symbiosis
keratin
dietary adaptation
Tineola bisselliella
url https://www.mdpi.com/2076-2607/8/9/1415
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