Comprehensive Physiology Wiley Online Library

Nutrient Absorption in Invertebrates

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Modes of Nutrient Absorption
1.1 Types of Absorption
1.2 Carrier‐Mediated Transport
2 Mechanisms of Soluble Nutrient Absorption
2.1 Diffusion
2.2 Facilitated Diffusion
2.3 Primary Active Transport
2.4 Secondary Active Transport
3 Kinetic and Energetic Aspects of Nutrient Transport
3.1 Kinetics
3.2 Energetics
4 Sites of Nutrient Absorption
4.1 Gastrointestinal Absorption
4.2 Integumental Absorption
5 Experimental Systems Employed for the Measurement of Nutrient Transport
5.1 Intacf Animals
5.2 Isolated Tissues
5.3 Isolated Cells
5.4 Cultured Cells
5.5 Subcellular Membrane Preparations
6 Nutrient Transport in Molluscs
6.1 Alimentary Nutrient Absorption
6.2 Integumental Nutrient Absorption
7 Nutrient Transport in Annelids
7.1 Alimentary Nutrient Absorption
7.2 Integumental Nutrient Absorption
7.3 General Characteristics of Integumental Transport in Annelids
7.4 Nutritional Role of Integumental Uptake in Marine Annelids
8 Nutrient Transport in Echinoderms
8.1 Alimentary Nutrient Absorption
8.2 Integumental Nutrient Absorption
9 Nutrient Transport in Coelenterates
9.1 Alimentary Transport
9.2 Integumental Transport
10 Nutrient Transport in Arthropods
10.1 Nutrient Transport in Insects
10.2 Nutrient Transport in Crustaceans
11 Conclusion
Figure 1. Figure 1.

Na‐gradient model of transepithelial glucose transport, modified from Crane . Glucose is transported across the apical membrane into the cell, against its electrochemical gradient, and coupled to a cotransport with Na, which moves down its electrochemical gradient. It then moves out of the cell into the blood, across the basolateral membrane, and down its electrochemical gradient. The Na gradient is maintained by removing the cotransported Na from the cell by means of an ATP‐requiring Na, K‐exchange pump (Na, K‐ATPase) in the basolateral membrane. Apical Na‐glucose co‐transport is an example of secondary active transport. Carrier‐mediated efflux of glucose across the basolateral membrane is representative of facilitated diffusion. ATP‐driven efflux of Na from the cell is an example of primary active transport.

Figure 2. Figure 2.

Hypothetical time course of nutrient uptake into an isolated tissue (A). Open circles represent uptake into a tissue free of extracellular space artifacts. The slope of the first several time points, during the linear phase of uptake reflecting the true unidirectional “initial rate” of transport, extrapolates back to the origin. Open squares represent uptake into a tissue that either rapidly binds the substrate, in addition to transporting a fraction into the cells, or has a geometry that results in trapping a volume extracellular medium that is not washed away during normal rinsing and blotting. The slope of the initial rate of uptake into the cells is equal to that noted in the lower curve; however, the line extrapolates back to a positive intercept, whose value reflects the amount of labeled substrate bound to the tissue or trapped in the extracellular space. (B) If the uptake into these two different tissues were to be based upon a single time point, the presence of the “bound volume” (open square) would result in a substantial overestimate of the true rate of cellular uptake.

Figure 3. Figure 3.

Influence of a poorly rinsed extracellular compartment on the measurement of kinetics of integumental transport in bivalve gill tissue. Uptake of 14C‐cycloleucine was measured in gills isolated from M. californianus (lateral cilia were not active). Data points represent uptake reflecting total retention of labeled substrate as the external concentration of cycloleucine was increased. The line labeled mediated uptake was calculated from the data for total uptake according to equation (see text) using nonlinear regression analysis. Jmax was 4.4 μmol · g−1 · h−1 and Kt was 66 μM. The first‐order component of uptake, D, was 3 nmol · g−1 · h−1M (dashed line). The experimentally determined extracellular volume (determined from retention of radiolabeled inulin) was equivalent to a first‐order accumulation of 3.2 nmol · g−1 · h−1M (dotted line).

Data modified from Wright and Stephens
Figure 4. Figure 4.

A family of curves showing the hypothetical Hill relationship (see equation ) between external Na+ concentration and rate of integumental nutrient transport. The three curves show the effect of having one, two, or three Na ions involved in catalytic activation of transport. For the purpose of this set of calculations, a K50 of 150 mM Na and a Jmax of 50 arbitrary units was assumed to be in effect for all three curves. Inset shows actual data for the influence of external Na on the activation of 1 μM taurine transport into M. californianus gill. Calculated Hill coefficient was 3.2, with a K50 and Jmax of 370 μM and 19.3 pmol · mg−1 · 2 min−1, respectively.

From Silva and Wright
Figure 5. Figure 5.

Computer‐generated contour plots showing the steady‐state concentration of taurine in the water stream flowing between adjacent gill filaments (depicted in cross‐section as rectangles) as a result of the normal efflux of taurine from the gill in the absence (A) and presence (B) of normal integumental taurine transport activity. Incoming (inhalant) seawater was assumed to contain no taurine. Heavy arrows show direction of water flow, from the frontal toward the abfrontal aspect of gill filaments. Calculations used the convection—diffusion model for determining the relationship between water flow and transport activity . The following values were used in calculations: peak flow velocity of 0.12 cm · s−1, a taurine “leak” of 4 × 10−4 mol · cm−2 · s−1, and in the case where transport was active, a Jmax of 4 × 10−12 mol · cm−2 · s−1 and a Kt of 1.5 μM.

From Wright and Secomb
Figure 6. Figure 6.

Diagram of basic subdivisions of insect alimentary canal. Shaded parts are ectodermal in origin and are lined with cuticle; unshaded parts are derived from endodermal tissues without a cuticular lining.

After Chapman
Figure 7. Figure 7.

Model for amino acid absorption across intestinal cells of lepidopteran larvae. A goblet cell between two columnar cells is indicated. Solid arrow indicates amino acid carrier system; open arrow represents K‐pump. Apical K‐pump of goblet cells maintains the cation at a cell brush border as a result of probable cell‐cell coupling, providing a favorable K diffusion gradient from lumen to cytoplasm and an adequate driving force for cytoplasmic amino acid accumulation by cotransport. Vs, trans‐serosal electrical potential difference; Vm, transmucosal electrical potential difference; Vms, transepithelial electrical potential difference. Since the cell interior is electrically negative with respect to external compartments, polarities are defined as follows: Vs, cell to hemolymph; Vm, lumen to cell; Vms, lumen to hemolymph. Values of electrical potential differences and potassium activities refer to Bombyx mori in vivo.

After Giordana et al.
Figure 8. Figure 8.

Hypothetical diagram of circulatory patterns of hepatopancreatic (digestive gland) fluid and chyme in the decapod proventriculus based on the model developed by Powell [] as applied to penaeid shrimp. Dotted lines, path of solid food; solid lines, path of fluid. AC, anterior chamber; AD, anterior diverticulum of midgut; DG, digestive gland opening; FP, filter‐press; LG, lateral grooves; MG, midgut; O, ossicles of gastric mill; OES, esophagus; PC, posterior chamber, PCG, dorsolateral grooves of posterior chamber; VG, ventral grooves.

From Dall and Moriarty
Figure 9. Figure 9.

Schematic drawings of transition zone and B‐cell zone in crayfish hepatopancreas tubule showing major cell types and differential ultrastructure. Different cell lines are represented by B, F, and R. ac, apical complex; bi, basal invaginations; bl, basal lamina; cm, circular muscle fiber; cv, clear vesicle; dv, dense‐core vesicle; Fe, iron granule in supranuclear vacuole; gly, glycogen; gol, Golgi body; HEM, hemolymph surrounding tubule; ld, lipid droplet; lm, longitudinal muscle fiber; LU, lumen of tubule; myo, cells are presumed functionally differentiated into absorptive and secretory roles, respectively. Differentiations of R‐ and F‐cell types (dashed lines) interact with movements of nutrients distally and digestive juices proximally (solid lines). Relative zone lengths are not drawn to scale.

After Loizzi
Figure 10. Figure 10.

Diagrammatic scheme of digestive physiology in crayfish hepatopancreas tubule. Precursor cells in the distal tip of each tubule for F cells and R cells undergo extensive mitotic division and migrate proximally. Differentation into these two cell lines occurs in the transition zone. In the B‐cell zone, F cells transform into B cells by enlargement of the supranuclear vacuole. Mature R and B cells are presumed functionally differentiated into absorptive and sectetory roles, respectively. Differentiations of R‐ and F‐cell types (dashed lines) interact with movements of nutrients distally and digestive juices proximally (solid lines). Relative zone lengths are not drawn to scale.

After Loizzi
Figure 11. Figure 11.

Model of hepatopancreatic R cell from Penaeus semisulcatus showing proposed routes of metabolite transport, storage, or degradation. Soluble substances are taken up at the apical cell membrane by diffusion of some carrier‐mediated transport system. Routes IA and IB: Soluble substances, including amino acids, simple sugars, lipid precursors, and ions, move into cell and follow route 1–7, marked by solid black arrows. These are channeled through smooth endoplasmic reticulum, rough endoplasmic reticulum, and Golgi systems, where a fraction is probably synthesized directly into lipid, glycogen, and protein. Residual material moves via multivesicular bodies to be incorporated in supranuclear vacuole. Both soluble and insoluble substances, including particulate ion and thorium dioxide, are taken up through the basal membrane. Routes HA and IIB: Soluble substances move into cell and flow via smooth endoplasmic reticulum and cytoplasmic inclusions to supranuclear vacuole. Route IIC: Insoluble macromolecules and particles are taken up by pinocytosis and eventually transported to the supranuclear vacuole, where they accumulate. b.l., basal lamina; c.i., cytoplasmic inclusions; d.b., dense body; e.c., enteric coat; Fe, particles of iron; g, Golgi bodies; mv, microvilli; m.v.b., mutivesicular body; p.v., pinocytotic vesicle; r.e.r., rough endoplasmic reticulum; s.e.r., smooth endoplasmic reticulum; s.n.v., supranuclear vacuole; v, vesicle.

After Al‐Mohanna and Nott
Figure 12. Figure 12.

Sodium‐dependent and sodium‐independent carrier‐mediated nutrient transport mechanisms of crustacean hepatopancreatic epithelial brush‐border membrane. Figure shows approximate transapical pH gradient in vivo, anticipated substrate charges resulting from protonation at physiologically acidic luminal pH, and proposed driving forces influencing transmembrane movements of each organic solute. Direction of arrows indicates whether a substrate is moving against or down an electrochemical gradient during transport across the brush‐border membrane.

From Ahearn et al.


Figure 1.

Na‐gradient model of transepithelial glucose transport, modified from Crane . Glucose is transported across the apical membrane into the cell, against its electrochemical gradient, and coupled to a cotransport with Na, which moves down its electrochemical gradient. It then moves out of the cell into the blood, across the basolateral membrane, and down its electrochemical gradient. The Na gradient is maintained by removing the cotransported Na from the cell by means of an ATP‐requiring Na, K‐exchange pump (Na, K‐ATPase) in the basolateral membrane. Apical Na‐glucose co‐transport is an example of secondary active transport. Carrier‐mediated efflux of glucose across the basolateral membrane is representative of facilitated diffusion. ATP‐driven efflux of Na from the cell is an example of primary active transport.



Figure 2.

Hypothetical time course of nutrient uptake into an isolated tissue (A). Open circles represent uptake into a tissue free of extracellular space artifacts. The slope of the first several time points, during the linear phase of uptake reflecting the true unidirectional “initial rate” of transport, extrapolates back to the origin. Open squares represent uptake into a tissue that either rapidly binds the substrate, in addition to transporting a fraction into the cells, or has a geometry that results in trapping a volume extracellular medium that is not washed away during normal rinsing and blotting. The slope of the initial rate of uptake into the cells is equal to that noted in the lower curve; however, the line extrapolates back to a positive intercept, whose value reflects the amount of labeled substrate bound to the tissue or trapped in the extracellular space. (B) If the uptake into these two different tissues were to be based upon a single time point, the presence of the “bound volume” (open square) would result in a substantial overestimate of the true rate of cellular uptake.



Figure 3.

Influence of a poorly rinsed extracellular compartment on the measurement of kinetics of integumental transport in bivalve gill tissue. Uptake of 14C‐cycloleucine was measured in gills isolated from M. californianus (lateral cilia were not active). Data points represent uptake reflecting total retention of labeled substrate as the external concentration of cycloleucine was increased. The line labeled mediated uptake was calculated from the data for total uptake according to equation (see text) using nonlinear regression analysis. Jmax was 4.4 μmol · g−1 · h−1 and Kt was 66 μM. The first‐order component of uptake, D, was 3 nmol · g−1 · h−1M (dashed line). The experimentally determined extracellular volume (determined from retention of radiolabeled inulin) was equivalent to a first‐order accumulation of 3.2 nmol · g−1 · h−1M (dotted line).

Data modified from Wright and Stephens


Figure 4.

A family of curves showing the hypothetical Hill relationship (see equation ) between external Na+ concentration and rate of integumental nutrient transport. The three curves show the effect of having one, two, or three Na ions involved in catalytic activation of transport. For the purpose of this set of calculations, a K50 of 150 mM Na and a Jmax of 50 arbitrary units was assumed to be in effect for all three curves. Inset shows actual data for the influence of external Na on the activation of 1 μM taurine transport into M. californianus gill. Calculated Hill coefficient was 3.2, with a K50 and Jmax of 370 μM and 19.3 pmol · mg−1 · 2 min−1, respectively.

From Silva and Wright


Figure 5.

Computer‐generated contour plots showing the steady‐state concentration of taurine in the water stream flowing between adjacent gill filaments (depicted in cross‐section as rectangles) as a result of the normal efflux of taurine from the gill in the absence (A) and presence (B) of normal integumental taurine transport activity. Incoming (inhalant) seawater was assumed to contain no taurine. Heavy arrows show direction of water flow, from the frontal toward the abfrontal aspect of gill filaments. Calculations used the convection—diffusion model for determining the relationship between water flow and transport activity . The following values were used in calculations: peak flow velocity of 0.12 cm · s−1, a taurine “leak” of 4 × 10−4 mol · cm−2 · s−1, and in the case where transport was active, a Jmax of 4 × 10−12 mol · cm−2 · s−1 and a Kt of 1.5 μM.

From Wright and Secomb


Figure 6.

Diagram of basic subdivisions of insect alimentary canal. Shaded parts are ectodermal in origin and are lined with cuticle; unshaded parts are derived from endodermal tissues without a cuticular lining.

After Chapman


Figure 7.

Model for amino acid absorption across intestinal cells of lepidopteran larvae. A goblet cell between two columnar cells is indicated. Solid arrow indicates amino acid carrier system; open arrow represents K‐pump. Apical K‐pump of goblet cells maintains the cation at a cell brush border as a result of probable cell‐cell coupling, providing a favorable K diffusion gradient from lumen to cytoplasm and an adequate driving force for cytoplasmic amino acid accumulation by cotransport. Vs, trans‐serosal electrical potential difference; Vm, transmucosal electrical potential difference; Vms, transepithelial electrical potential difference. Since the cell interior is electrically negative with respect to external compartments, polarities are defined as follows: Vs, cell to hemolymph; Vm, lumen to cell; Vms, lumen to hemolymph. Values of electrical potential differences and potassium activities refer to Bombyx mori in vivo.

After Giordana et al.


Figure 8.

Hypothetical diagram of circulatory patterns of hepatopancreatic (digestive gland) fluid and chyme in the decapod proventriculus based on the model developed by Powell [] as applied to penaeid shrimp. Dotted lines, path of solid food; solid lines, path of fluid. AC, anterior chamber; AD, anterior diverticulum of midgut; DG, digestive gland opening; FP, filter‐press; LG, lateral grooves; MG, midgut; O, ossicles of gastric mill; OES, esophagus; PC, posterior chamber, PCG, dorsolateral grooves of posterior chamber; VG, ventral grooves.

From Dall and Moriarty


Figure 9.

Schematic drawings of transition zone and B‐cell zone in crayfish hepatopancreas tubule showing major cell types and differential ultrastructure. Different cell lines are represented by B, F, and R. ac, apical complex; bi, basal invaginations; bl, basal lamina; cm, circular muscle fiber; cv, clear vesicle; dv, dense‐core vesicle; Fe, iron granule in supranuclear vacuole; gly, glycogen; gol, Golgi body; HEM, hemolymph surrounding tubule; ld, lipid droplet; lm, longitudinal muscle fiber; LU, lumen of tubule; myo, cells are presumed functionally differentiated into absorptive and secretory roles, respectively. Differentiations of R‐ and F‐cell types (dashed lines) interact with movements of nutrients distally and digestive juices proximally (solid lines). Relative zone lengths are not drawn to scale.

After Loizzi


Figure 10.

Diagrammatic scheme of digestive physiology in crayfish hepatopancreas tubule. Precursor cells in the distal tip of each tubule for F cells and R cells undergo extensive mitotic division and migrate proximally. Differentation into these two cell lines occurs in the transition zone. In the B‐cell zone, F cells transform into B cells by enlargement of the supranuclear vacuole. Mature R and B cells are presumed functionally differentiated into absorptive and sectetory roles, respectively. Differentiations of R‐ and F‐cell types (dashed lines) interact with movements of nutrients distally and digestive juices proximally (solid lines). Relative zone lengths are not drawn to scale.

After Loizzi


Figure 11.

Model of hepatopancreatic R cell from Penaeus semisulcatus showing proposed routes of metabolite transport, storage, or degradation. Soluble substances are taken up at the apical cell membrane by diffusion of some carrier‐mediated transport system. Routes IA and IB: Soluble substances, including amino acids, simple sugars, lipid precursors, and ions, move into cell and follow route 1–7, marked by solid black arrows. These are channeled through smooth endoplasmic reticulum, rough endoplasmic reticulum, and Golgi systems, where a fraction is probably synthesized directly into lipid, glycogen, and protein. Residual material moves via multivesicular bodies to be incorporated in supranuclear vacuole. Both soluble and insoluble substances, including particulate ion and thorium dioxide, are taken up through the basal membrane. Routes HA and IIB: Soluble substances move into cell and flow via smooth endoplasmic reticulum and cytoplasmic inclusions to supranuclear vacuole. Route IIC: Insoluble macromolecules and particles are taken up by pinocytosis and eventually transported to the supranuclear vacuole, where they accumulate. b.l., basal lamina; c.i., cytoplasmic inclusions; d.b., dense body; e.c., enteric coat; Fe, particles of iron; g, Golgi bodies; mv, microvilli; m.v.b., mutivesicular body; p.v., pinocytotic vesicle; r.e.r., rough endoplasmic reticulum; s.e.r., smooth endoplasmic reticulum; s.n.v., supranuclear vacuole; v, vesicle.

After Al‐Mohanna and Nott


Figure 12.

Sodium‐dependent and sodium‐independent carrier‐mediated nutrient transport mechanisms of crustacean hepatopancreatic epithelial brush‐border membrane. Figure shows approximate transapical pH gradient in vivo, anticipated substrate charges resulting from protonation at physiologically acidic luminal pH, and proposed driving forces influencing transmembrane movements of each organic solute. Direction of arrows indicates whether a substrate is moving against or down an electrochemical gradient during transport across the brush‐border membrane.

From Ahearn et al.
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Stephen H. Wright, Gregory A. Ahearn. Nutrient Absorption in Invertebrates. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 1137-1205. First published in print 1997. doi: 10.1002/cphy.cp130216