Duplications and Functional Convergence of Intestinal Carbohydrate-Digesting Enzymes

Abstract

Vertebrate diets and digestive physiologies vary tremendously. Although the contribution of ecological and behavioral features to such diversity is well documented, the roles and identities of individual intestinal enzymes shaping digestive traits remain largely unexplored. Here, we show that the sucrase-isomaltase (SI)/maltase-glucoamylase (MGAM) dual enzyme system long assumed to be the conserved disaccharide and starch digestion framework in all vertebrates is absent in many lineages. Our analyses indicate that independent duplications of an ancestral SI gave rise to the mammalian-specific MGAM, as well as to other duplicates in fish and birds. Strikingly, the duplicated avian enzyme exhibits similar activities to MGAM, revealing an unexpected case of functional convergence. Our results highlight digestive enzyme variation as a key uncharacterized component of dietary diversity in vertebrates.

Sucrose digestion capacity in birds shows convergent coevolution with nectar composition across continents

“…High sucrase activities per unit intestinal surface area more than compensate for the reduced intestinal surface area and length that has been repeatedly documented in nectar-feeding birds ( Richardson and Wooller, 1986 ; Wooller and Richardson 1988 ). Sucrase activity is owing to the action of a membrane-bound alpha-glucosidase enzyme called sucrase-isomaltase (coded by the SI gene) and expressed in the apical membrane of intestinal cells (called the brush-border membrane, Brun et al., 2020a ). Recently developed methods in proteomics allow quantifying the abundance of different digestive enzymes in the brush-border membrane ( Brun et al., 2020b ).…”

“…Recently developed methods in proteomics allow quantifying the abundance of different digestive enzymes in the brush-border membrane ( Brun et al., 2020b ). These proteomics methods have revealed that in the muscicapoid lineage (predominantly insectivorous) that includes starlings, thrushes, and mockingbirds, sucrase is present ( Brun et al., 2020a ) but has lost the ability to hydrolyze sucrose ( Martínez del Rio, 1990b ). In this light, we hypothesized that the abundance of the sucrose-isomaltase protein in the intestinal brush-border membrane is higher in nectarivorous birds than in other birds.…”

“…Although the abundance of sucrase in the intestinal brush-border is likely an important contributor to the capacity to hydrolyze sucrose, it might not be the only factor that leads to higher sucrase capacity in nectar-feeding birds. Unlike mammals that have two discrete alpha-glucosidases with distinct, but partially overlapping, substrate specificities ( Brun et al., 2020a ), the birds that we studied have sucrose-isomaltase as the sole intestinal enzyme capable of hydrolyzing sucrose, maltose and isomaltose. We found that maltose hydrolysis capacity scaled positively with body mass (F2,38 = 53.46, p < 0.0001, Figure 4 A).…”

“…Here, we focus on one of these potentially convergent traits: sucrose digestion rate at the brush-border membrane of intestinal cells. To be assimilated, the disaccharide sucrose must be hydrolyzed into its monosaccharide components glucose and fructose by a membrane-bound intestinal α-glucosidase enzyme called sucrase-isomaltase (henceforth “sucrase,” Brun et al., 2020a ). The capacity to digest sucrose, defined as the rate at which the whole intestine hydrolyses sucrose, limits maximal food intake in hummingbirds ( McWhorter and Martínez del Rio, 2000 ).…”

Understanding the early ontogenetic stages of Mugil liza (Mugilidae): Morphological traits and digestive/metabolic profile of pre‐juveniles after recruitment

“…Data are the mean ± activity was found in early and late pre-juveniles. This suggests that this activity could correspond to a sucrase-independent maltaseglucoamylase complex (Bertucci et al, 2019;Brun et al, 2020;Chaudet et al, 2019;Dhital et al, 2013;Morelos-Castro et al, 2020).…”