Weevil carbohydrate intake triggers endosymbiont proliferation: a trade-off between host benefit and endosymbiont burden

Abstract

Nutritional symbiosis between insects and intracellular bacteria (endosymbionts) are a major force of adaptation, allowing animals to colonize nutrient-poor ecological niches. Many beetles feeding on tyrosine-poor substrates rely on a surplus of aromatic amino acids produced by bacterial endosymbionts that synthesize them autotrophically. This surplus of aromatic amino acids is crucial for the biosynthesis of a thick exoskeleton, the cuticle, which is made of a matrix of chitin with proteins and pigments built from the tyrosine-derived 3,4-dihydroxyphenylalanine (DOPA14), providing an important defensive barrier against biotic and abiotic stress. Other endosymbiont-related advantages for beetles include a faster development, and improved fecundity. The association between the cereal weevil Sitophilus oryzae and Sodalis pierantonius endosymbiont19 represents a unique case study: in young adult weevils, endosymbionts undergo a massive proliferation concomitant with the cuticle tanning, then they are fully eliminated. While endosymbiont clearance is a host-controlled process, the mechanism triggering endosymbiont proliferation remains poorly understood. Here, we show that endosymbiont proliferation relies on host carbohydrate intake. Remarkably, insect fecundity was preserved, and the cuticle tanning achieved, even when endosymbiont proliferation was experimentally blocked, except in the context of a severely unbalanced diet. Moreover, a high endosymbiont load coupled with nutrient shortage dramatically impacts host survival, revealing the high energy cost of proliferating endosymbionts and the incapacity of the host to adjust energy allocation.

Transcriptional survey of ovarian bacteriomes in the cereal weevil,Sitophilus oryzae, shows down-regulation of immune effectors at the onset of sexual maturity

“…In these conditions, the timespan between egg laying and the emergence of adults from the grain is one month. Adults emerging from the grain are fully formed, although their cuticle is reinforced during the two-three days following emergence (Vigneron et al, 2014; Dell’Aglio et al, 2022), together with sexual maturation (Perez-Mendoza et al, 2004; Dell’Aglio et al, 2022). The time between the end of metamorphosis and emergence has been calculated to be around three to four days (Vigneron et al, 2014; Dell’Aglio et al, 2022).…”

“…Three biological samples per time point were collected, each composed of 10 ovarian systems. Flow cytometry was performed exactly as described previously (Dell'Aglio et al, 2022).…”

“…In the cereal weevil Sitophilus oryzae , endosymbionts are housed within a bacteriome located at the larval foregut-midgut junction, in many bacteriomes at the apex of adult midgut caeca, as well as at the apex of female ovaries (Figure 1A). In young adult weevils, an exponential increase in endosymbionts was observed in midgut bacteriomes during the first week of adulthood (Vigneron et al, 2014), triggered by the host carbohydrate intake (Dell’Aglio et al, 2022). The drastic increase in endosymbiont load is accompanied by an increase in the bacteriome-specific AMP ColA (Masson et al, 2015a), and was shown to provide aromatic amino acids necessary for the host cuticle maturation (Vigneron et al, 2014).…”

“…The bottom-right image shows bacteria in the germarium, outside of the bacteriome (D7). C-D. Quantification of endosymbiont load by flow cytometry in ovaries and gut (gut from (Dell’Aglio et al, 2022)). Endosymbiont load increases in the first couple of days in both ovaries and gut bacteriomes, although there are a hundred times more in the gut.…”

Transcriptomic-based selection of reference genes for quantitative real-time PCR in an insect endosymbiotic model

“…Error bars represent standard deviation. Bacterial dynamics is represented in the bottom right corner, adapted from (Dell’Aglio et al, 2022).…”