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

Abstract

The evolutionary success of insects is promoted by their association with beneficial microbes that enable the utilization of unusual diets. The synanthropic clothing moth Tineola bisselliella 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 Bacillus 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 T. bisselliella 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.

Next-Generation Sequencing Analysis of the Tineola bisselliella Larval Gut Transcriptome Reveals Candidate Enzymes for Keratin Digestion

“…This might indicate a limited role for symbionts in the T. bisselliella larval gut, or may reflect a peculiarity of the samples we analyzed in our experiments. In line with a recent study reporting the presence of a new Bacillus species in the T. bisselliella larval gut [22], we identified a few contigs with similarities to bacterial keratinases. Further analysis of the T. bisselliella larval microbiome should identify the species that need to be evaluated in more detail to address the role of microbial keratinases in the dietary preferences of clothes moths.…”

“…Although data on the gut microbiome of the clothes moth are inconsistent, most reports could not identify abundant gut bacteria in T. bisselliella larvae [2,[20][21][22]. We investigated the taxonomic profile of the assembly by comparing all predicted ORFs (94,304) to the UniProt database.…”

“…Most keratinases described thus far originate from bacteria, but the T. bisselliella larval gut is not inhabited by a persistent microbial community even though some recently identified species of Bacillus may contribute to keratin degradation [20][21][22]. Keratin degradation mechanisms have been reported for bacteria and fungi [23].…”

Keratinases as Versatile Enzymatic Tools for Sustainable Development

“…Every year, new microorganisms and microbial strains with keratin-degrading abilities are isolated from various environments, including feather waste landfills, skin surface, soil and water bodies near slaughterhouses, industrial wastewaters and organisms such as insects and spiders [ 39 , 42 ].…”

Nutritional Properties of Larval Epidermis and Meat of the Edible Insect Clanis bilineata tsingtauica (Lepidoptera: Sphingidae)

“…The possibility of using edible insects as food and feed was suggested in 1975 as a route to easing global food shortages [ 2 , 3 ] and has also been addressed by the Food and Agricultural Organization (FAO) [ 4 , 5 ]. Although insects are the largest and most diverse group of organisms on Earth, their implementation as a food source has not been fully utilized [ 6 , 7 ]. Over one million species of named insects are estimated to exist worldwide, and approximately 1900–2000 species are edible [ 8 , 9 , 10 ].…”