Postprandial morphological response of the intestinal epithelium of the Burmese python (Python molurus)

Abstract

The postprandial morphological changes of the intestinal epithelium of Burmese pythons were examined using fasting pythons and at eight time points after feeding. In fasting pythons, tightly packed enterocytes possess very short microvilli and are arranged in a pseudostratified fashion.Enterocyte width increases by 23% within 24 h postfeeding, inducing significant increases in villus length and intestinal mass. By 6 days postfeeding, enterocyte volume had peaked, following as much as an 80% increase. Contributing to enterocyte hypertrophy is the cellular accumulation of lipid droplets at the tips and edges of the villi of the proximal and middle small intestine, but were absent in the distal small intestine. At 3 days postfeeding, conventional and environmental scanning electron microscopy revealed cracks and lipid extrusion along the narrow edges of the villi and at the villus tips. Transmission electron microscopy demonstrated the rapid postprandial lengthening of enterocyte microvilli, increasing 4.8-fold in length within 24 h, and the maintaining of that length through digestion. Beginning at 24 h postfeeding, spherical particles were found embedded apically within enterocytes of the proximal and middle small intestine. These particles possessed an annular-like construction and were stained with the calcium-stain Alizarine red S suggesting that they were bone in origin. Following the completion of digestion, many of the postprandial responses were reversed, as observed by the atrophy of enterocytes, the shortening of villi, and the retraction of the microvilli. Further exploration of the python intestine will reveal the underlying mechanisms of these trophic responses and the origin and fate of the engulfed particles.

Adaptive regulation of digestive performance in the genusPython

“…Plausible mechanisms for enterocyte hypertrophy include the mobilization of amino acids from protein sources for enterocyte rebuilding and the absorption of luminal nutrients. Although there is no current evidence to support the former explanation, the latter explanation is well supported from observations of enterocytes of P. molurus filled with lipid droplets originating from the meal (Starck and Beese, 2001;Lignot et al, 2005). Our histological examinations revealed the presence of lipid droplets within enterocytes of fed snakes in all of the five python species.…”

“…First, the Burmese python Python molurus has been the focus of a collection of studies on physiological responses to feeding and fasting (Secor and Diamond, 1995; Stark and Beese, 2001;Overgaard et al, 1999;Lignot et al, 2005). With feeding, P. molurus experiences dramatic increases in metabolic rate, cardiac output, gastric acid production, intestinal nutrient transport and hypertrophy of the small intestine (Secor and Diamond, 1995;Secor and Diamond, 1997;Secor, 2003;Lignot et al, 2005). Upon the completion of digestion, these postprandial responses are reversed; metabolism is depressed, gastric acid production ceases, intestinal nutrient transport is downregulated, and the intestine atrophies.…”

“…For each of these organisms, the increase in small intestinal mass is largely attributed to the thickening of the intestinal mucosa, which results from villus lengthening, itself a product of enterocyte hypertrophy. For pythons and estivating anurans, enterocyte width and volume increase with feeding by 40-90% and 50-440%, respectively (Cramp and Franklin, 2005;Lignot et al, 2005;Secor, 2005b). In addition to enterocyte hypertrophy, cellular hyperplasia (replication) may also contribute to the postprandial increase in intestinal mass.…”

“…In addition to enterocyte hypertrophy, cellular hyperplasia (replication) may also contribute to the postprandial increase in intestinal mass. However, for P. molurus, the postprandial increases in enterocyte replication are matched by a concurrent increase in apoptosis (Lignot and Secor, 2003;Lignot et al, 2005). Hence, the postprandial increase in python intestinal mass appears largely to be a product of cellular hypertrophy rather than hyperplasia.…”

Digesting pythons quickly oxidize the proteins in their meals and save the lipids for later

“…Within 24 h of ingestion of a meal, a python's small intestine doubles in mass (Secor, 1995;Secor and Diamond, 1995;Lignot et al, 2005) and volume (Hansen et al, 2013), and increases its mass-specific lipid content by 75% (Henriksen et al, 2015). A portion of this increase in lipid content is caused by the accumulation of lipid droplets in the apical side of the enterocytes during the first day of digestion (Starck and Beese, 2001;Lignot et al, 2005;Starck and Wimmer, 2005;Helmstetter et al, 2009). It is generally believed that the meal is the primary source of these lipids (Holmberg et al, 2003;Starck and Wimmer, 2005;Secor, 2008;Henriksen et al, 2015), but this phenomenon has not been formally documented using any tracer methods.…”