Insects Recycle Endosymbionts when the Benefit Is Over

• Published in: Current biology Vol. 24; no. 19; pp. 2267 - 2273
• Main Authors: Vigneron, Aurélien, Masson, Florent, Vallier, Agnès, Balmand, Séverine, Rey, Marjolaine, Vincent-Monégat, Carole, Aksoy, Emre, Aubailly-Giraud, Etienne, Zaidman-Rémy, Anna, Heddi, Abdelaziz
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 06.10.2014; Elsevier
• Subjects: Animals; Bacterial Proteins - genetics; Electron Transport Complex I - genetics; Enterobacteriaceae - genetics; Enterobacteriaceae - metabolism; Enterobacteriaceae - physiology; Female; Larva - microbiology; Life Sciences; Male; Molecular Sequence Data; Pupa - microbiology; Real-Time Polymerase Chain Reaction; Sequence Analysis, DNA; Sitophilus; Sodalis; Symbiosis; Weevils - growth & development; Weevils - microbiology
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2014.07.065

Symbiotic associations are widespread in nature and represent a driving force in evolution. They are known to impact fitness, and thereby shape the host phenotype [1–4]. Insects subsisting on nutritionally poor substrates have evolved mutualistic relationships with intracellular symbiotic bacteria (endosymbionts) that supply them with metabolic components lacking in their diet [5–10]. In many species, endosymbionts are hosted within specialized host cells, called the bacteriocytes, and transmitted vertically across host generations [11]. How hosts balance the costs and benefits of having endosymbionts, and whether and how they adjust symbiont load to their physiological needs, remains largely unexplored. By investigating the cereal weevil Sitophilus association with the Sodalis pierantonius endosymbiont [8, 12], we discover that endosymbiont populations intensively multiply in young adults, before being rapidly eliminated within few days. We show that young adults strongly depend on endosymbionts and that endosymbiont proliferation after metamorphosis matches a drastic host physiological need for the tyrosine (Tyr) and phenylalanine (Phe) amino acids to rapidly build their protective exoskeleton. Tyr and Phe are precursors of the dihydroxyphenylalanine (DOPA) molecule that is an essential component for the cuticle synthesis. Once the cuticle is achieved, DOPA reaches high amounts in insects, which triggers endosymbiont elimination. This elimination relies on apoptosis and autophagy activation, allowing digestion and recycling of the endosymbiont material. Thus, the weevil-endosymbiont association reveals an adaptive interplay between metabolic and cellular functions that minimizes the cost of symbiosis and speeds up the exoskeleton formation during a critical phase when emerging adults are especially vulnerable. [Display omitted] •Weevil endosymbionts drastically multiply after adult molting, before being eliminated•Symbiosis is required for a rapid synthesis of the adult protective cuticle•Endosymbionts are promptly recycled by autophagy once the cuticle is achieved•DOPA accumulation parallels symbiont elimination and cuticle completion Vigneron et al. report that weevil endosymbionts intensively multiply in young adults to support a rapid cuticle formation, before being promptly recycled. Symbiont load adjustment to host nutritional needs involves interplays between metabolism and autophagy and optimizes the cost of endosymbionts and their impacts on host physiological traits.