The gastric proton pump in gobiid and mudskipper fishes. Evidence of stomach loss?

ABSTRACT

Stomach loss has occurred independently multiple times during gnathostome evolution with notable frequency within the Teleostei. Significantly, this loss of acid-peptic digestion has been found to correlate with the secondary genomic loss of the gastric proton pump subunits (atp4a, atp4b) and pepsinogens/pepsins (pga, pgc). Gastric glands produce gastric juice containing the acid and pepsin and thus their presence is a hallmark feature of a digestive system capable of acid-peptic digestion. However, in gobiid fishes although oesogaster and gastric glands have been identified histologically, their functional significance has been questioned. In the present study we address whether the gastric proton pump is present and expressed in gastric glands of the goby Neogobius species (Gobiidae) and in members of the family Oxudercidae, a group of amphibious gobiid fishes commonly known as mudskippers (genera Periophthalmus, Boleophthalmus, Periophthalmodon and Scartelaos). We confirmed the presence of gastric glands and have immunohistochemically localized gastric proton pump expression to these glands in Neogobius fluviatilis and Periophthalmus novemradiatus, Periophthalmus barbarus and Boleophthalmus boddarti. Genome analysis in Neogobius melanostomus, Periophthalmus magnuspinnatus, Scartelaos histophorus, Boleophthalmus pectinirostris, and Periophthalmodon schlosseri revealed the presence of both atp4a and atp4b subunit orthologues in all species in a conserved genomic loci organization. Moreover, it was possible to deduce that the complete open reading frame and the key functional amino acid residues are present. The conserved expression of the gastric proton pump provides clear evidence of the potential for gastric acid secretion indicating that acid digestion is retained in these gobiid fishes and not lost.