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Background: Mutualistic interactions with microbes can help insects adapt to extreme environments and unusual diets. An intriguing example is the burying beetle Nicrophorus vespilloides, which feeds and reproduces on small vertebrate carcasses. Its fungal microbiome is dominated by yeasts that potentially facilitate carcass utilization by producing digestive enzymes, eliminating cadaver-associated toxic volatiles (that would otherwise attract competitors), and releasing antimicrobials to sanitize the microenvironment. Some of these yeasts are closely related to the biotechnologically important species Yarrowia lipolytica., Results: To investigate the roles of these Yarrowia-like yeast (YLY) strains in more detail, we selected five strains from two different phylogenetic clades for third-generation sequencing and genome analysis. The first clade, represented by strain B02, has a 20-Mb genome containing ~ 6400 predicted protein-coding genes. The second clade, represented by strain C11, has a 25-Mb genome containing ~ 6300 predicted protein-coding genes, and extensive intraspecific variability within the ITS-D1/D2 rDNA region commonly used for species assignments. Phenotypic microarray analysis revealed that both YLY strains were able to utilize a diverse range of carbon and nitrogen sources (including microbial metabolites associated with putrefaction), and can grow in environments with extreme pH and salt concentrations., Conclusions: The genomic characterization of five yeast strains isolated from N. vespilloides resulted in the identification of strains potentially representing new YLY species. Given their abundance in the beetle hindgut, and dominant growth on beetle-prepared carcasses, the analysis of these strains has revealed the genetic basis of a potential symbiotic relationship between yeasts and burying beetles that facilitates carcass digestion and preservation.

Microbial symbionts of herbivorous insects have been suggested to aid in the detoxification of plant defense compounds; however, quantitative studies on microbial contribution to plant toxin degradation remain scarce. Here, we demonstrate microbiome-mediated degradation of plant-derived toxic isothiocyanates in the cabbage stem flea beetle Psylliodes chrysocephala, a major pest of oilseed rape. Suppression of microbiota in antibiotic-fed beetles resulted in up to 11.3-fold higher levels of unmetabolized isothiocyanates compared to control beetles but did not affect other known detoxification pathways in P. chrysocephala. We characterized the microbiome of laboratory-reared and field-collected insects using 16S rRNA amplicon sequencing and isolated bacteria belonging to the three core genera Pantoea, Acinetobacter and Pseudomonas. Only Pantoea isolates rapidly degraded isothiocyanates in vitro, and restored isothiocyanate degradation in vivo when reintroduced in antibiotic-fed beetles. Pantoea was consistently present across beetle life stages and in field and lab populations. In addition, Pantoea was detected in undamaged tissues of the host plant Brassica rapa, indicating that P. chrysocephala could possibly acquire an isothiocyanate detoxifying bacterium through their diet. Our results demonstrate that both insect endogenous mechanisms and the microbiota can contribute to the detoxification of plant defense compounds and together they can better account for the fate of ingested plant metabolites., (© 2020 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

The ability to feed on a wide range of diets has enabled insects to diversify and colonize specialized niches. Carrion, for example, is highly susceptible to microbial decomposers, but is kept palatable several days after an animal's death by carrion-feeding insects. Here we show that the burying beetle Nicrophorus vespilloides preserves carrion by preventing the microbial succession associated with carrion decomposition, thus ensuring a high-quality resource for their developing larvae. Beetle-tended carcasses showed no signs of degradation and hosted a microbial community containing the beetles' gut microbiota, including the yeast Yarrowia In contrast, untended carcasses showed visual and olfactory signs of putrefaction, and their microbial community consisted of endogenous and soil-originating microbial decomposers. This regulation of the carcass' bacterial and fungal community and transcriptomic profile was associated with lower concentrations of putrescine and cadaverine (toxic polyamines associated with carcass putrefaction) and altered levels of proteases, lipases, and free amino acids. Beetle-tended carcasses develop a biofilm-like matrix housing the yeast, which, when experimentally removed, leads to reduced larval growth. Thus, tended carcasses hosted a mutualistic microbial community that promotes optimal larval development, likely through symbiont-mediated extraintestinal digestion and detoxification of carrion nutrients. The adaptive preservation of carrion coordinated by the beetles and their symbionts demonstrates a specialized resource-management strategy through which insects modify their habitats to enhance fitness., Competing Interests: The authors declare no conflict of interest., (Copyright © 2018 the Author(s). Published by PNAS.)

Necrophagous beetles utilize carrion, a highly nutritious resource that is susceptible to intense microbial competition, by treating it with antimicrobial anal and oral secretions. However, how this regulates the carcass microbiota remains unclear. Here, we show that carcasses prepared by the burying beetle Nicrophorus vespilloides undergo significant changes in their microbial communities subsequent to their burial and "preparation." Prepared carcasses hosted a microbial community that was more similar to that of beetles' anal and oral secretions than to the native carcass community or the surrounding soil, indicating that the beetles regulated the carcass microbiota. A core microbial community (Xanthomonadaceae, Enterococcaceae, Enterobacteriaceae and Yarrowia yeasts) was transmitted by the beetles to the larvae via the anal and oral secretions and the carcass surface. These core taxa proliferated on the carcass, indicating a growth conducive environment for these microbes when associated with beetles. However, total bacterial loads were higher on decomposing carcasses without beetles than on beetle-prepared carcasses, indicating that the beetles and/or their associated symbionts suppress the growth of competing microbes. Thus, apart from being a nutritional resource, the carcass provides a medium for vertical transmission of a tightly regulated symbiotic microbiota, whose activity on the carcass and in the larval gut may involve carcass preservation as well as digestion., (© 2017 John Wiley & Sons Ltd.)

Insects that use ephemeral resources must rapidly digest nutrients and simultaneously protect them from competitors. Here we use burying beetles (Nicrophorus vespilloides), which feed their offspring on vertebrate carrion, to investigate the digestive and defensive basis of carrion utilization. We characterize gene expression and microbiota composition in the gut, anal secretions, and on carcasses used by the beetles. We find a strict functional compartmentalization of the gut involving differential expression of immune effectors (antimicrobial peptides and lysozymes), as well as digestive and detoxifying enzymes. A distinct microbial community composed of Firmicutes, Proteobacteria and a clade of ascomycetous yeasts (genus Yarrowia) is present in larval and adult guts, and is transmitted to the carcass via anal secretions, where the yeasts express extracellular digestive enzymes and produce antimicrobial compounds. Our results provide evidence of potential metabolic cooperation between the host and its microbiota for digestion, detoxification and defence that extends from the beetle's gut to its nutritional resource.

Vertebrate dung is central to the dung beetle life cycle, constituting food for adults and a protective and nutritive refuge for their offspring. Adult dung beetles have soft mandibles and feed primarily on nutritionally rich dung particles, while larvae have sclerotized mandibles and consume coarser dung particles with a higher C/N ratio. Here, using the dung beetles Euoniticellus intermedius and E. triangulatus, we show that these morphological adaptations in mandibular structure are also correlated with differences in basic gut structure and gut bacterial communities between dung beetle life stages. Metagenome functional predictions based on 16S rDNA characterization further indicated that larval gut communities are enriched in genes involved in cellulose degradation and nitrogen fixation compared to adult guts. Larval gut communities are more similar to female gut communities than they are to those of males, and bacteria present in maternally provisioned brood balls and maternal 'gifts' (secretions deposited in the brood ball along with the egg) are also more similar to larval gut communities than to those of males. Maternal secretions and maternally provisioned brood balls, as well as dung, were important factors shaping the larval gut community. Differences between gut microbiota in the adults and larvae are likely to contribute to differences in nutrient assimilation from ingested dung at different life history stages., (© 2016 John Wiley & Sons Ltd.)