Department of Forest and Wildlife Ecology, Russell Laboratories, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.
PLoS One. 2012;7(2):e32417. doi: 10.1371/journal.pone.0032417. Epub 2012 Feb 28.
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 (M(r) = 150.1 Da) and lactulose (M(r) = 342.3 Da). We also measured absorption of labeled 3-O-methyl-D-glucose (3OMD-glucose; M(r) = 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.
植物次生代谢物（SMs）普遍存在于动物食品中，可能会影响动物的摄食行为、种间相互作用以及动物的分布和丰度。植物中次生代谢物的主要类别包括许多在分子大小范围内的水溶性化合物，这些化合物可以通过扩散或溶剂拖曳穿过肠上皮细胞的细胞旁空间。不同物种之间的细胞旁通透性存在差异。使用含有次生代谢物的中东啮齿动物和鸟类消费者，我们测试了这样一个假设，即鸟类的细胞旁通透性将明显高于啮齿动物。完整动物的通透性通过使用标准药理学方法来评估，以测量两种惰性、中性、水溶性示踪剂的吸收，这些示踪剂不与肠道营养转运体相互作用，分别是 L-阿拉伯糖（Mr = 150.1 Da）和乳果糖（Mr = 342.3 Da）。我们还测量了 3-O-甲基-D-葡萄糖（3OMD-葡萄糖；Mr = 194.2 Da）的吸收，3OMD-葡萄糖是 D-葡萄糖的非代谢类似物，通过细胞旁空间被动吸收，但也穿过肠细胞的细胞膜进行转运。大多数葡萄糖被所有物种吸收，但在鸟类中，阿拉伯糖的分数吸收（f）几乎是啮齿动物的三倍（鸟类中 1.03±0.17，n = 15 种中有 2 种；啮齿动物中 0.37±0.06，n = 10 种中有 2 种）（P<0.001）。令人惊讶的是，鸟类中阿拉伯糖的表观吸收速率超过了 3OMD-葡萄糖。我们的发现与先前的研究结果一致，表明与非飞行哺乳动物相比，鸟类中细胞旁途径更为突出，并表明鸟类可能会受到水溶性膳食次生代谢物更大吸收的挑战。鸟类中细胞旁途径的表达增加暗示着一种权衡：鸟类通过被动吸收水溶性营养素获得的自由能可能会被它们为了消除同时吸收的次生代谢物而产生的代谢需求所抵消。
