The role of the gut microbiome in mediating standard metabolic rate after dietary shifts in the viviparous cockroach,Diploptera punctata

Abstract

Diet may be a significant determinant of insect gut microbiome composition. However, the extent to which dietary shifts shape both the composition and relevant functions of insect gut microbiomes, and ultimately impact host energy balance (i.e. metabolic phenotype), is not well understood. We investigated the impacts of diet switching on Diploptera punctata females maintained on a dog food (DF) diet relative to those fed a comparatively sub-optimal cellulose-amended dog food (CADF) diet for 4 weeks. After this period, dietary shift resulted in a significantly higher average mass-specific standard metabolic rate (SMR) in CADF-fed females compared with DF-fed females. We also uncovered significant 13 C-enrichment in DF-fed insect samples relative to CADF-fed insect samples and lowered bacterial essential amino acid (EAA) provisioning in CADF-fed samples. Differences in SMR and EAA provisioning were not accompanied by significant differences in overall microbiome composition between the two groups. However, cellulolytic and nitrogen-fixing bacterial families dominant in wild omnivorous cockroaches and wood-feeding termites were significantly enriched in CADF-fed females than in DF-fed females, at the end of the study. We propose that these changes in microbiome composition after dietary shifts are associated with changes in EAA provisioning and possibly SMR. Further studies are needed to comprehensively understand the relative importance of gut microbial functions among the complexity of factors known to underscore SMR responses in insects under varying dietary conditions.

Larval nutrition impacts survival to adulthood, body size and the allometric scaling of metabolic rate in adult honeybees

“…However, physiological adaptations to imbalanced diets, such as increasing gut length, may be metabolically costly (Yang and Joern, 1994). The few studies that have examined the impact of manipulating the nutritional composition of diets have generally found that nutritionally poor diets elevate average RMR (Zanotto et al, 1997;Ayayee et al, 2018Ayayee et al, , 2020; but see Clark et al, 2016). Typically, these studies considered short-term impacts of diet on metabolism during either adulthood or a single juvenile stage, ignoring the impact of the nutritional composition of diets on the scaling of RMR with body mass or size.…”

“…A recent study found that adult stick insects exhibit developmental diet-dependent differences in RMR when reared from birth on leaves from plant species varying in their nutritional content and digestibility (Hill et al, 2020), but the impact of developmental diet on the scaling of RMR and body mass was not considered. Shorter term studies conducted in adult insects only are more common, and have typically observed a reduction in RMR in response to a nutritionally poor diet (Zanotto et al, 1997;Ayayee et al, 2018Ayayee et al, , 2020; but see Clark et al, 2016).…”

Different Gut Microbiomes of Developmental Stages of Field-Collected Native and Invasive Western Bean Cutworm, Striacosta albicosta, in Western Nebraska

“…Finally, members of the bacterial order Pseudomonadales (Pseudomonadaceae and Moraxellaceae; class Gammaproteobacteria) were also abundant in eggs and adults and to a lesser extent in larvae. Several bacterial orders and families under the class gammaproteobacteria are recognized members of the gut microbiome across several insect species, serving as providers of metabolic nitrogen [3,46,47], essential amino acids [4,44], and microbe-derived hydrolytic enzymes [45,46]. These representative taxa may be performing similar functions in S. albicosta.…”

“…The past two decades have seen a tremendous increase in the availability of data detailing the microbial compositions of the gut microbiomes of various insects and the postulated functions of these gut microbiomes [1,2]. In some particular instances, the functions of insect gut microbiomes have been demonstrated to include nitrogen provisioning [3], essential amino acid provisioning [4][5][6][7], and an overall propensity for essential nutrient provisioning followed by detoxification and digestion [8]. These functions have been uncovered in both insect species considered pests and non-pests.…”

Larval nutrition impacts survival to adulthood, body size, and the allometric scaling of metabolic rate in adult honeybees

“…A recent study found that adult stick insects exhibit developmental diet dependent differences in RMR when reared from birth on leaves from plant species varying in their nutritional content and digestibility (Hill, Silcocks and Andrew, 2020), but the impact of developmental diet on the scaling of RMR and body mass was not considered. Shorter term studies conducted in adult insects only are more common, and have typically observed a reduction in RMR in response to a lower quality diet (Zanotto et al ., 1997; Ayayee et al ., 2018, 2020, but see Clark, Zera and Behmer, 2016).…”