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Ecological Physiology of Diet and Digestive Systems

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Ecological Physiology of Diet and Digestive Systems PH73CH04-Karasov ARI 3 January 2011 9:50 Ecological Physiology of Diet and Digestive Systems William H. Karasov,1,∗ Carlos Martınez´ del Rio,2 and Enrique Caviedes-Vidal3 1Department of Forest and Wildlife Ecology, University of Wisconsin, Madison, Wisconsin 53706; email: [email protected] 2Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming 82070; email: [email protected] 3Departamento de Bioquımica´ y Ciencias Biologicas,´ Universidad Nacional de San Luis and Instituto Multidisciplinario de Investigaciones Biologicas´ de San Luis, Consejo Nacional de Investigaciones Cientıficas´ y Tecnicas,´ 5700 San Luis, Argentina; email: [email protected] Annu. Rev. Physiol. 2011. 73:69–93 Keywords The Annual Review of Physiology is online at adaptation, hydrolases, transporters, microbiome physiol.annualreviews.org This article’s doi: Abstract 10.1146/annurev-physiol-012110-142152 The morphological and functional design of gastrointestinal tracts of Copyright c 2011 by Annual Reviews. by University of Wyoming on 02/14/11. For personal use only. many vertebrates and invertebrates can be explained largely by the in- All rights reserved teraction between diet chemical constituents and principles of economic 0066-4278/11/0315-0069$20.00 design, both of which are embodied in chemical reactor models of gut Annu. Rev. Physiol. 2011.73:69-93. Downloaded from www.annualreviews.org ∗Corresponding author. function. Natural selection seems to have led to the expression of diges- tive features that approximately match digestive capacities with dietary loads while exhibiting relatively modest excess. Mechanisms explain- ing differences in hydrolase activity between populations and species include gene copy number variations and single-nucleotide polymor- phisms. In many animals, both transcriptional adjustment and posttran- scriptional adjustment mediate phenotypic flexibility in the expression of intestinal hydrolases and transporters in response to dietary signals. Digestive performance of animals depends also on their gastrointestinal microbiome. The microbiome seems to be characterized by large beta diversity among hosts and by a common core metagenome and seems to differ flexibly among animals with different diets. 69 PH73CH04-Karasov ARI 3 January 2011 9:50 INTRODUCTION large variation among foods in both types and amounts of materials refractory (i.e., re- Resource acquisition is a basic task of all an- sistant) to digestion, in the types of main nu- Microbiota: all imals, and animals have diversified tremen- tritional substrates (e.g., simple and complex microbes in a dously to make use of the full bounty offered carbohydrates, proteins, fats), and in compo- well-defined by the Earth’s biodiversity. In this review, we environment sition within each substrate type (e.g., spe- discuss digestive features of animals (and their cific bond linkages, chain length differences) microbiota) that eat a wide variety of food types. (Table 1). Substrate types require different par- Our goal is to present some of the general ques- ticular complements of secretions and enzymes tions, modes of research, and findings that span for their breakdown and particular mechanisms and define the field. We build on many fine ear- for the absorption of their breakdown prod- lier reviews (1–6). Our focus is on physiologi- ucts. The time course over which those prod- cal matches with diet among species that might ucts are released and absorbed varies widely be classified as specialists and thus “major” on among food and substrate types. Accordingly, certain food types (i.e., the majority of what it the foods at the top of Table 1 are com- eats is a single food type) and those species that posed mainly of sugars, protein, and lipids are omnivores (eat a variety of foods) or make that can be broken down relatively rapidly physiological adjustments as they switch among by typical enzymatic activities (disaccharidases, foods of different composition. Owing to space amylases, proteases, peptidases, lipases) present limitations, we do not review the literature on endogenously in the digestive tracts of most an- digestive physiology changes in response to in- imals. But as one scans down Table 1, the food creased/decreased energy demands or to onto- types have increasing amounts of material, such genetic changes in diet. But even after those as plant cell wall or arthropod cuticle/chitin, exclusions, the vast diversity of animals and di- that is refractory to rapid digestion with en- ets forces our coverage of digestive systems in dogenous enzymes. At the bottom of Table 1, relation to diets to be extensive rather than in- the dry mass of woody vegetation, fungi, and tensive, and so we selectively discuss some of detritus may be composed of 75% or more re- the best and/or most recent examples. fractory cell wall material. We begin with three unifying principles in Some animals consume foods that contain the ecological physiology of diet and digestive low amounts of refractory material (e.g., top systems. These principles play out in all three of Table 1), and some of those animals’ key major sections that follow: matches achieved digestive adaptations described below are hy- between diet and digestion (a) in catalytic di- by University of Wyoming on 02/14/11. For personal use only. drolytic or absorptive capacities that match the gesters (animals that rely on endogenous en- relative amounts of carbohydrate, protein, and zymes for digestion), (b) in animals that adjust fat in their diets. But among animals that con- Annu. Rev. Physiol. 2011.73:69-93. Downloaded from www.annualreviews.org to changes in diet composition, and (c)inani- sume refractory food types near the bottom of mals that rely on their microbiota in digestion. Table 1, there are multiple strategies. Within many taxonomic groups, there are species that KEY PRINCIPLES IN THE “skim the cream,” assimilate cell contents or STUDY OF DIETS AND other nonrefractory materials, and pass the re- DIGESTIVE SYSTEMS fractory material mainly undigested. Abe & Higashi (7) referred to them as cytoplasm Variation in Food Chemistry Drives consumers and contrasted them with other Diversification of Digestive Systems species termed cell wall consumers, which ex- Features of food chemistry ultimately drive tract considerable energy from refractory ma- diversification of digestive system morphol- terials. Among herbivorous mammals, these ogy, physiology, and biochemistry. There is two extremes are exemplified by, respectively, 70 Karasov · Mart´ınez del Rio · Caviedes-Vidal PH73CH04-Karasov ARI 3 January 2011 9:50 Table 1 Diet items, some of their key chemical components, and enzymes required to break them downa Enzyme activitiesb Refractory materials or Less refractory Diet item(s) chemical(s) chemical(s) 1 2 3 4 5 6 7 8 9 10 11 Nectar Nil Simple sugars Milk Nil Lactose Animal flesh Nil Glycogen Insects, zooplankton Cuticle, chitin Glycogen, trehalose Bacteria peptidoglycan in G(+) Soluble bacterial cell walls polysaccharides Terrestrial plant materials Celluloses,c lignin, insoluble Sucrose, starch (flowers, seeds, fruits, starchesd leaves, twigs) Aquatic/marine plant Celluloses, mannanes, xylans, Starch, laminarin, www.annualreviews.org materials (green & brown, agarose and by University of Wyoming on 02/14/11. For personal use only. diatoms, seaweeds) chrysolaminarine Plant exudates (saps, resins, Phenols and terpene Sucrose Annu. Rev. Physiol. 2011.73:69-93. Downloaded from www.annualreviews.org latexes, gums) derivatives, hemicellulose, other complex β-linked polysaccharides • Physiology of Diet and Digestive Systems 71 Fungi and lichens N-Acetyl-β-D- glucoaminides, N bound to cell wall components Detritus Celluloses, lignin, xylans, Starches, α-glucans mannanes aThis table is not comprehensive and lists only the main types of food items discussed in this article. The diet items are ranked (top to bottom) in approximate order of the relative amounts of material in them that is refractory to digestion (low to high). In both vertebrates and invertebrates, digestive efficiency tends to be inversely related to the amount of refractory material in a food (2). bA diamond symbol represents the presence of enzyme activity. Enzyme activities include the following: (1) Proteases and peptidases, which hydrolyze oligopeptides formed by proteases (2) Ester bond hydrolases (e.g., lipase, phospholipase) (3–5) α-Glucosidases: (3) α-amylases (hydrolyzes starch from plants and glycogen from animals), (4) α-glucosidases [e.g., maltase (hydrolyzes the oligosaccharides formed by amylase), sucrase (hydrolyzes sucrose from plants), oligodisaccharidases], (5) trehalase (hydrolyzes trehalose, the principal blood sugar in insects) (6–9) β-Glucosidases: (6) lactase, (7) cellulase (cellulose is hydrolyzed by the concerted action of three types of cellulases: endocellulases, exocellulases, and β-glucosidases), (8) xylanase and pectinase, (9) laminarinase (exo-1,3,-β-glucanases that hydrolyze the major storage polysaccharides in brown algae, laminarin, and chrysolaminarin) (10) Chitinases (11) Lysozyme [hydrolyzes peptidoglycan in G(+) bacterial cell walls (58)] cCellulose and hemicellulose. dThe crystalline pattern of starch seems to determine its susceptibility to hydrolysis (176). eβ-1,3-glucan storage products (laminarin) (52). PH73CH04-Karasov ARI 3 January 2011 9:50 giant pandas (Ailuropoda melanoleuca), which di- Models Help Reduce the Complexity gest less than 10% of cellulose
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