Capacity for Absorption of Water-Soluble Secondary Metabolites Greater in Birds than in Rodents

William H Karasov,Bradley Hartman Bakken,Enrique Caviedes-Vidal,Michal Samuni-Blank,Ido Izhaki,Zeev Arad,Brock Fenton

doi:10.1371/journal.pone.0032417

Abstract

Plant secondary metabolites (SMs) are pervasive in animal foods and potentially influence feeding behavior, interspecies interactions, and the distribution and abundance of animals. Some of the major classes of naturally occurring SMs in plants include many water-soluble compounds in the molecular size range that could cross the intestinal epithelium via the paracellular space by diffusion or solvent drag. There are differences among species in paracellular permeability. Using Middle Eastern rodent and avian consumers of fruits containing SMs, we tested the hypothesis that avian species would have significantly higher paracellular permeability than rodent species. Permeability in intact animals was assessed using standard pharmacological methodology to measure absorption of two radiolabeled, inert, neutral water-soluble probes that do not interact with intestinal nutrient transporters, L-arabinose (Mr = 150.1 Da) and lactulose (Mr = 342.3 Da). We also measured absorption of labeled 3-O-methyl-D-glucose (3OMD-glucose; Mr = 194.2 Da), which is a nonmetabolized analogue of D-glucose that is passively absorbed through the paracellular space but also transported across the enterocyte membranes. Most glucose was absorbed by all species, but arabinose fractional absorption (f) was nearly three times higher in birds (1.03±0.17, n = 15 in two species) compared to rodents (0.37±0.06, n = 10 in two species) (P<0.001). Surprisingly, the apparent rates of absorption in birds of arabinose exceeded those of 3OMD-glucose. Our findings are in agreement with previous work showing that the paracellular pathway is more prominent in birds relative to nonflying mammals, and suggests that birds may be challenged by greater absorption of water-soluble, dietary SMs. The increased expression of the paracellular pathway in birds hints at a tradeoff: the free energy birds gain by absorbing water-soluble nutrients passively may be offset by the metabolic demands placed on them to eliminate concomitantly absorbed SMs.

Highlights

Secondary metabolites (SMs) are compounds produced and/or sequestered by plants and animals that do not appear to play a major role in their primary nutritional or regulatory metabolism
Lipophilic SMs are anticipated to permeate intestinal cell membranes passively at rates positively related to their octanol or oil:water partition coefficients [3], their rates might be decreased by complexing proteins [4,5], physical barriers [6,7,8], and membrane transporters that bind them and export them back into the lumen [9,10,11]
Recoveries of probes injected into A. cahirinus were: L-arabinose, 8465% (n = 4; Fig. 1A); L-lactulose, 9662% (n = 4; 1B); 3-O-methyl-Dglucose, 10061% (n = 4; 1C)

Summary

Introduction

Secondary metabolites (SMs) are compounds produced and/or sequestered by plants and animals that do not appear to play a major role in their primary nutritional or regulatory metabolism. Their functions include communication, attraction, or defense against herbivores, predators, pathogens, and competitors [1]. The tight junctions adjoining adjacent enterocytes have selective permeability, discriminating among solutes by charge and size [14] In both eutherian mammal and avian species the paracellular route of passive absorption of water-soluble compounds has been visualized by either autoradiography [15] or confocal laser microscopy [16,17]. For example, has a MW of 162 Da, its cationic forms are water soluble, and it was found to be absorbed by the paracellular pathway in cell culture (TR146 cells) [23]

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Conclusion