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Microbiome-assisted carrion preservation aids larval development in a burying beetle

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Significance Ephemeral diets such as carrion are high-quality resources that are susceptible to microbial spoilage. Carrion-feeding insects that breed on decaying carcasses must overcome challenges arising from competing microbes. Here… Click to show full abstract

Significance Ephemeral diets such as carrion are high-quality resources that are susceptible to microbial spoilage. Carrion-feeding insects that breed on decaying carcasses must overcome challenges arising from competing microbes. Here we report that a carrion-feeding burying beetle preserves carcasses by regulating its microbial growth, resulting in changes in its biochemical properties including the reduction of toxic polyamines associated with putrefaction and nutrient loss. The beetle’s microbial symbionts form a biofilm-like matrix on carcasses, which is important for optimal larval development. The beetles and their microbiome thus coordinate a specialized adaptive strategy of carrion management, enabling them to preserve carrion quality and support larval growth in a challenging resource such as carrion. 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.

Keywords: carrion; insects; larval development; burying beetle

Journal Title: Proceedings of the National Academy of Sciences of the United States of America
Year Published: 2018

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