Intestinal paracellular absorption is necessary to support the sugar oxidation cascade in nectarivorous bats

Abstract

We made the first measurements of the capacity for paracellular nutrient absorption in intact nectarivorous bats. Leptonycteris yerbabuenae (20 g mass) were injected with or fed inert carbohydrate probes L-rhamnose and D(+)-cellobiose, which are absorbed exclusively by the paracellular route, and 3-O-methyl-Dglucose (3OMD-glucose), which is absorbed both paracellularly and transcellularly. Using a standard pharmacokinetic technique, we collected blood samples for 2 h after probe administration. As predicted, fractional absorption ( f ) of paracellular probes declined with increasing M r in the order of rhamnose ( f=0.71)>cellobiose ( f=0.23). Absorption of 3OMD-glucose was complete ( f=0.85; not different from unity). Integrating our data with those for glucose absorption and oxidation in another nectarivorous bat, we conclude that passive paracellular absorption of glucose is extensive in nectarivorous bat species, as in other bats and small birds, and necessary to support high glucose fluxes hypothesized for the sugar oxidation cascade.

Sugar Metabolism in Hummingbirds and Nectar Bats

“…Instead, a paracellular transport mechanism accounts for most of the movement of sugar across the intestinal epithelium [ 16 ] ( Figure 1 ). Nectar bats also have high levels of intestinal sucrase, allowing hydrolysis of sucrose contained in nectars and fruits [ 17 ], and make use of a predominantly paracellular pathway for intestinal sugar absorption [ 18 ]. Hummingbirds and nectar bats ingesting sugars display digestive efficiencies close to 100% [ 12 , 15 ].…”

“…Values increase up to 30 mM after feeding on sucrose solutions and return close to fasted, resting values as a result of exercise after meals [ 69 ]. Because both hummingbirds and nectar bats make primary use of the paracellular route in transporting glucose and fructose across the intestinal wall [ 16 , 18 ], differences in flight muscle GLUT expression ( Figure 6 ) offer a likely explanation for the differences in blood glucose kinetics. It appears likely that the ability to restore low concentrations of blood glucose in nectar bats is at least partly the consequence of GLUT4 recruitment and elevated rates of glucose uptake and phosphorylation in the flight muscles in response to insulin and exercise [ 44 ].…”

“…The mechanisms by which hummingbirds and nectar bats routinely hover at mass-specific V values about ten- and fivefold higher, respectively, than those of human athletes exercising at V max have been the subject of continuing investigation [ 2 , 63 , 84 ]. While the paracellular pathway plays a minor role in biomedical models, e.g., [ 85 ], it plays a dominant role, accounts for most of the intestinal glucose absorption in nectarivorous animals and operates at rates high enough to supply the fuel requirements of muscles during flight [ 16 , 18 ].…”

Small nutrient molecules in fruit fuel efficient digestion and mutualism with plants in frugivorous bats

“…The absorption of small nutrient molecules, such as simple sugars, free amino acids, and peptides, occurs directly through the paracellular and transcellular pathways 57,58 . The first is important in bats 56,59 . Food rich in small nutrient molecules should result in a fast and high assimilation, even with short intestines, as we observed.…”