Date Published: March 12, 2018
Publisher: Public Library of Science
Author(s): Alexandre Lobo-da-Cunha, Diogo Amaral-de-Carvalho, Elsa Oliveira, Ângela Alves, Vítor Costa, Gonçalo Calado, Etsuro Ito.
Mannitol oxidase and polyol dehydrogenases are enzymes that convert polyalcohols into sugars. Mannitol oxidase was previously investigated in terrestrial snails and slugs, being also present in a few aquatic gastropods. However, the overall distribution of this enzyme in the Gastropoda was not known. Polyol dehydrogenases are also poorly studied in gastropods and other mollusks. In this study, polyalcohol oxidase and dehydrogenase activities were assayed in the digestive gland of 26 species of gastropods, representing the clades Patellogastropoda, Neritimorpha, Vetigastropoda, Caenogastropoda and Heterobranchia. Marine, freshwater and terrestrial species, including herbivores and carnivores were analyzed. Ultrastructural observations were undertake in species possessing mannitol oxidase, in order to investigate the correlation between this enzyme and the presence of tubular structures known to be associated with it. Mannitol oxidase activity was detected in the digestive gland of herbivores from the clades Caenogastropoda and Heterobranchia, but not in any carnivores or in herbivores from the clades Patellogastropoda, Neritimorpha and Vetigastropoda. In most of the species used in this study, dehydrogenase activities were detected using both D-mannitol and D-sorbitol as substrates. Nevertheless, in some carnivores these activities were not detected with both polyalcohols. Ultrastructural observations revealed tubular structures in digestive gland cells of some species having mannitol oxidase activity, but they were not observed in others. Based on our results, we suggest that mannitol oxidase first occurred in a herbivorous or omnivorous ancestor of Apogastropoda, the clade formed by caenogastropods and heterobranchs, being subsequently lost in those species that shifted towards a carnivorous diet.
Mannitol oxidase and polyol dehydrogenases are enzymes that convert polyalcohols into sugars. Mannitol oxidase catalyzes the conversion of D-mannitol into D-mannose using molecular oxygen as hydrogen acceptor, releasing hydrogen peroxide . This enzyme is known in terrestrial slugs and snails [2, 3], and in a few aquatic gastropods , but its overall distribution in the Gastropoda remained unknown. NAD+ is the hydrogen acceptor for polyol dehydrogenases, which are well known in animals, fungi, plants and prokaryotes. These enzymes belong to the medium-chain dehydrogenases/reductases (MDR) superfamily that include several alcohol dehydrogenases [5, 6]. Although sorbitol dehydrogenase was reported in the digestive gland of the freshwater snail Viviparus viviparus , polyol dehydrogenases are still poorly investigated in mollusks, the second largest phylum of multicellular animals. To contribute for filling these gaps in knowledge, we started by measuring oxidase and dehydrogenase activities in the digestive gland of several gastropods using mannitol and sorbitol as substrates.