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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 115; no. 44; pp. 11274 - 11279
• Main Authors: Shukla, Shantanu P., Plata, Camila, Reichelt, Michael, Steiger, Sandra, Heckel, David G., Kaltenpoth, Martin, Vilcinskas, Andreas, Vogel, Heiko
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 30-10-2018
• Subjects: Amino acids; Animals; Bacteria - metabolism; Beetles; Biodegradation; Biofilms; Biofilms - growth & development; Biological Sciences; Cadaverine; Cadaverine - metabolism; Carcasses; Carrion; Coleoptera - growth & development; Coleoptera - microbiology; Communities; Decomposition; Detoxification; Fitness; Fungi; Fungi - metabolism; Housing; Insects; Intestinal microflora; Larva - growth & development; Larva - microbiology; Larvae; Larval development; Microbiomes; Microbiota; Microbiota - physiology; Microorganisms; Niches; Nicrophorus vespilloides; Nutrients; Polyamines; Preservation; Putrefaction; Putrescine; Putrescine - metabolism; Resource management; Symbionts; Symbiosis; Transcriptome - genetics; Yarrowia lipolytica; Yeast; insect nutrition; fungus; symbiosis; gut microbiota; resource competition
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1812808115

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.