Digesting pythons quickly oxidize the proteins in their meals and save the lipids for later

Abstract

Pythons digesting rodent meals exhibit up to 10-fold increases in their resting metabolic rate (RMR); this increase in RMR is termed specific dynamic action (SDA). Studies have shown that SDA is partially fueled by oxidizing dietary nutrients, yet it remains unclear whether the proteins and the lipids in their meals contribute equally to this energy demand. We raised two populations of mice on diets labeled with either [ 13 C]leucine or [ 13 C]palmitic acid to intrinsically enrich the proteins and lipids in their bodies, respectively. Ball pythons (Python regius) were fed whole mice (and pureed mice 3 weeks later), after which we measured their metabolic rates and the δ 13 C in the breath. The δ 13C values in the whole bodies of the protein-and lipid-labeled mice were generally similar (i.e. 5.7±4.7‰ and 2.8±5.4‰, respectively) but the oxidative kinetics of these two macronutrient pools were quite different. We found that the snakes oxidized 5% of the protein and only 0.24% of the lipids in their meals within 14 days. Oxidation of the dietary proteins peaked 24 h after ingestion, at which point these proteins provided ∼90% of the metabolic requirement of the snakes, and by 14 days the oxidation of these proteins decreased to nearly zero. The oxidation of the dietary lipids peaked 1 day later, at which point these lipids supplied ∼25% of the energy demand. Fourteen days after ingestion, these lipids were still being oxidized and continued to account for ∼25% of the metabolic rate. Pureeing the mice reduced the cost of gastric digestion and decreased SDA by 24%. Pureeing also reduced the oxidation of dietary proteins by 43%, but it had no effect on the rates of dietary lipid oxidation. Collectively, these results demonstrate that pythons are able to effectively partition the two primary metabolic fuels in their meals. This approach of uniquely labeling the different components of the diet will allow researchers to examine new questions about how and when animals use the nutrients in their meals.

More than just sugar: allocation of nectar amino acids and fatty acids in a Lepidopteran

“…This sustained 13 C enrichment in the breath suggests that nectar lipids provide a longer-term source of metabolic fuel than the amino acids. Similar differences in oxidative kinetics were observed in pythons consuming laboratory mice whose amino acids or fatty acids were labelled with 13 C [42]. The advanced technology that employs labelling of specific macronutrients on specific carbon atoms has enhanced our ability to track the fate of these macronutrients.…”

Stable isotope tracers reveal a trade‐off between reproduction and immunity in a reptile with competing needs

“…We found remarkable consistency between our two proxies of lipid stores: higher fat body scores assessed during laparotomy were associated with relatively higher investment of protein in self‐maintenance (Figures S2D and S4D), and higher C:N ratios (indicative of higher lipid content) of skin biopsies were associated with higher rates of protein excretion (Table S1) and relatively higher allocation to self‐maintenance (Figure e), both processes that animals can afford to prioritize only when ample stored energy is available to fuel future demands. In general, it seems that preserving stored energy whenever possible is an adaptive strategy, even for short‐lived organisms (Levin et al., ; McCue et al., ). In contrast, we found no evidence that variation in incoming food resources affected the allocation of protein to reproduction or self‐maintenance (Tables S1–S3).…”

“…McCue et al. () measured a 13 C label in breath CO 2 to show that quail spared protein from oxidation during the day but not at night, and McCue, Guzman, and Passement () used the same technique to describe how and when pythons use the proteins in their meals. Recently, Brace et al.…”

“…A few in vivo studies have examined the effects of starvation on metabolism (McCue et al, 2013), but none have traced amino acids to different, competing ultimate fates within the bodies of living organisms. McCue et al (2013) measured a 13 C label in breath CO 2 to show that quail spared protein from oxidation during the day but not at night, and McCue, Guzman, and Passement (2015) used the same technique to describe how and when pythons use the proteins in their meals. Recently, Brace et al (2015) used a 13 C label to trace the competing fates of fatty acids in Brown Anoles (Anolis sagrei), and Levin et al (2017) traced 13 C-labelled amino acids in sphingid tobacco hornworm moths (Manduca sexta) with this goal in mind.…”

The speed and metabolic cost of digesting a blood meal depends on temperature in a major disease vector

“…carbohydrates, lipids and amino acids) provided this energy. Indeed, the postprandial oxidative kinetics of different classes of nutrients have been studied in other animals including humans (Hoekstra et al, 1996;Labayen et al, 2004a,b), rodents , reptiles (McCue et al, 2015a) and birds (Swennen et al, 2007;McCue et al, 2010McCue et al, , 2011. These studies show that both dietary carbohydrates and proteins are readily used for immediate energy during digestion.…”