Relationships of RNA of intestinal carbohydrases and sugar transporters among vertebrate species

KARASOV, WILLIAM H.; AGUSTIN BARICALLA; MAGALLANES, MELISA E.; ANTONIO BRUN; CARLOS MARTINEZ DEL RIO; CAVIEDES-VIDAL E

San Diego

Congreso; Comparative physiology: From Organisms to Omics in an Uncertain World; 2022

American Physiological Society

We tested several predictions regarding relative gene expression ofkey proteins of the enterocytes, main intestinal cells involved indigestion of carbohydrate. The overarching hypothesis is that matchesevolve between dietary load of carbohydrate and intestinal activity ofthe enzymes and transporters that effect the digestion and uptake ofcarbohydrates by enterocytes. This match between digestive capacityand carbohydrate load has been observed both within species asindividuals shift between diets of contrasting nutrient composition(e.g., from low to high carbohydrate diets), and among species wherespecies with diets of differing macronutrient compositions exhibitpredictable differences in the activity of alpha-glucosidases (AGs) andintestinal sugar transporters. We previously showed that a primarymechanism accounting for variation in activity of intestinal hydrolasesis differences in gene expression (i.e., mRNA transcription) resulting indifferences in functional copies of coded proteins. Examples of this,which we refer to as “adaptive transcriptional control”, includeprimarily dietary modulation of hydrolytic activity within species, butcomparisons across species are sparse. Here we rely on the increasingnumber of publicly available published studies (SRA-NCBI) of intestinalgene expression to test for expected patterns among species, throughthe comparison of the normalized expression (by gene length andsequence depth). Consider for example, the apical (brush border)membrane enzyme sucrase-isomaltase (SI) that hydrolyzes -amongother substrates- sucrose releasing glucose and fructose. Among 27species of vertebrates including bony & cartilaginous fish, reptile,crocodile, bird and mammal, there are positive correlations betweenrelative expression of SI and genes for glucose transport such asSLC5A1 (SGLT1; P < 0.0001) and SGLT4 (P = 0.009). Among 23species, expression of the fructose transporter (SLC2A5) is alsopositively correlated with SI expression (P = 0.0072). Mammals alsoexpress another protein, MGAM, with maltase activity but withoutsucrase activity, and in an interesting contrast, the expression ofSLC2A5 is not correlated with MGAM expression in 10 mammal species(P > 0.7), whereas expression of SLC5A1 is correlated with MGAM.Free glucose absorbed into enterocytes is exported across their basallateral membrane towards blood via the glucose transporter GLUT2.Consistent with the previous patterns, expression of GLUT2 is alsopositively correlated with expression of SI. Trehalase, whichhydrolyzes trehalose from insect blood and fungi, releasing glucose,occurs in some species of most vertebrate classes except birds. Aswas the case for SI and MGAM, the expression of its gene TREH is alsocorrelated with expression of all the glucose transporters (SLC5A1,SLC5A9, SLC2A2). Hence, most of our tests were consistent with thehypothesis of “adaptive transcriptional control”. Supported byU.S.N.S.F (to WHK) and CONICET (to E.C.-V).