Is there a compromise between nutrient uptake and gas exchange in the gut of Misgurnus anguillicaudatus, an intestinal air-breathing fish?

Abstract

The Asian weatherloach, Misgurnus anguillicaudatus (Cobitidae), is a facultative air-breathing teleost fish that makes use of its hindgut or intestine as an accessory air-breathing organ (ABO). The hindgut is highly modified, being well vascularized with intraepithelial capillaries, which makes it well suited for gas exchange. However, the consequences for nutrient uptake, the traditional function of the intestine are unknown. The alimentary canal was examined histologically to assess differences between the fore-, mid- and hindgut regions that have been considered as the digestive, spiral and respiratory zones, respectively. In order to characterise the potential digestive (absorptive) function of the respiratory zone we used semi-quantitative polymerase chain reaction (PCR) to detect the presence of the intestinal Na(+):glucose cotransporter (SGLT1; SLC5A1) and H(+):peptide cotransporter (PEPT1a; SLC15A1) and partially sequenced the SGLT1 and PEPT1a cDNAs. These two transporters play important roles in the absorption of carbohydrate and di-/tripeptides, respectively, in the gut of fishes and other vertebrates and were therefore used as markers for potential nutrient uptake function. We also determined their tissue distributions through semi-quantitative RT-PCR. The effects of diet composition (high protein or high carbohydrate) or fasting on gene expression were also examined. SGLT1 expression was found in kidney, liver, heart, as well as in the three zones of the gut except the most distal part of the hindgut. PEPT1a mRNA was found in heart, brain, liver, and fore- and midgut, but absent in the hindgut. Our results clearly show high expression of SGLT1 (both mRNA and protein by immunolocalization) and PEPT1a (mRNA) in the foregut and midgut correlated with the digestive region of the gut. Modulatory effects of diet on the gene expression for both SGLT1 and PEPT1a were not observed. The presence of SGLT1 transcripts in the respiratory zone of the intestine suggests an overlap in function. However, in the case of PEPT1a, the distal limit was the midgut. Thus, despite its highly modified structure, the hindgut of the loach retains some potential nutrient uptake function.