Integrative Proteomic Analysis of Digestive Tract Glycosidases from the Invasive Golden Apple Snail, Pomacea canaliculata

Abstract

The freshwater snail Pomacea canaliculata, an invasive species of global significance, possesses a well-developed digestive system and diverse feeding mechanisms enabling the intake of a wide variety of food. The identification of glycosidases in adult snails would increase the understanding of their digestive physiology and potentially generate new opportunities to eradicate and/or control this invasive species. In this study, liquid chromatography coupled to tandem mass spectrometry was applied to define the occurrence, diversity, and origin of glycoside hydrolases along the digestive tract of P. canaliculata. A range of cellulases, hemicellulases, amylases, maltases, fucosidases, and galactosidases were identified across the digestive tract. The digestive gland and the contents of the crop and style sac yield a higher diversity of glycosidase-derived peptides. Subsequently, peptides derived from 81 glycosidases (46 proteins from the public database and 35 uniquely from the transcriptome database) that were distributed among 13 glycoside hydrolase families were selected and quantified using multiple reaction monitoring mass spectrometry. This study showed a high glycosidase abundance and diversity in the gut contents of P. canaliculata which participate in extracellular digestion of complex dietary carbohydrates. Salivary and digestive glands were the main tissues involved in their synthesis and secretion.

Antioxidant Responses Induced by Short-Term Activity–Estivation–Arousal Cycle in Pomacea canaliculata

“…The digestive gland of P. canaliculata is a key organ that participates in multiple and diverse physiological processes (Cowie, 2002;Hayes et al, 2015), and contains a bacterial symbiont in the digestive epithelial cells with detoxification and digestive functions (Castro-Vazquez et al, 2002;Vega et al, 2005Vega et al, , 2006Vega et al, , 2007Godoy et al, 2013;Campoy-Diaz et al, 2018Escobar-Correas et al, 2019). Compared to the respiratory organs, the digestive gland showed higher levels of ROS, equivalent levels of protein and lipid damage, and high SOD and CAT activities in estivating and aroused snails.…”

Composition and diversity of gut microbiota in Pomacea canaliculata in sexes and between developmental stages

“…Its capacity to process a broad variety of vegetable organic matter is due to the presence of cellulolytic enzymes, both from the gut microbiome and stomach of the snail [ 53 , 54 ]. The bacterial communities inside the gut of the snail may have crucial importance in the digestion of cellulose and other plant wall components [ 55 ]. Higher proportions of Proteobacteria and Firmicutes were often associated with diets containing plant ingredients [ 56 ].…”

Metagenomic analysis suggests unique gut‐microbiota composition and GH family constitution of Macrotermes annandalei

“…In Odontotermes yunnanensis, a large number of debranched enzymes and oligosaccharide degrading enzymes were identified, while cellulase and endoglucanase were minimal (Hojo 2019, Liu et al 2018, sharply contrasting to results in this study. Among GH enzymes in seven termites in Brazil, GH66, GH13, GH23 and GH18 are the most common gene families, while GH1 and GH9 were present in all the studies (Bai et al 2021, Escobar-Correas et al 2019, Grieco et al 2019, Jose et al 2017. Trinervitermes trinervoides has 14 gene families (Rashamuse et al 2016).…”

“…2021), golden apple snail (Escobar‐Correas et al . 2019), and higher termites (Marynowska et al . 2020).…”

“…This indicated that the GH7 enzymes are mainly present in protozoa symbiotic with lower termites. Other than intestinal microbes of M. annandalei, previous metagenomic studies of intestinal microbes in other animals were carried in Indian crossbred cattle (Jose et al 2017), Chinese bamboo rat (Bai et al 2021), golden apple snail (Escobar-Correas et al 2019), and higher termites (Marynowska et al 2020).…”