Proteomic analysis of digestive tract peptidases and lipases from the invasive gastropod Pomacea canaliculata

Abstract

Background: The invasive gastropod Pomacea canaliculata has received great attention in the last decades as a result of its negative impact on crops agriculture, yet knowledge of their digestive physiology remains incomplete, particularly the enzymaticbreakdown of macromolecules such as proteins and lipids.Results: Discovery proteomics revealed aspartic peptidases, cysteine peptidases, serine peptidases, metallopeptidases andthreonine peptidases, as well as acid and neutral lipases and phospholipases along the digestive tract of P. canaliculata. Peptides specific to peptidases (139) and lipases (14) were quantified by targeted mass spectrometry. Digestion begins in themouth via diverse salivary peptidases (nine serine peptidases; seven cysteine peptidases, one aspartic peptidase and 22 metallopeptidases) and then continues in the oesophagus (crop) via three luminal metallopeptidases (Family M12) and six serinepeptidases (Family S1). Downstream, the digestive gland provides a battery of enzymes composed of aspartic peptidase(one), cysteine peptidases (nine), serine peptidases (12) and metallopeptidases (24), including aminopeptidases, carboxypeptidases and dipeptidases). The coiled gut has M1 metallopeptidases that complete the digestion of small peptides. Lipid extracellular digestion is completed by triglyceride lipases.Conclusion: From an integrative physiological and anatomical perspective, P. canaliculata shows an unexpected abundanceand diversity of peptidases, which participate mainly in extracellular digestion. Moreover, the previously unknown occurrenceof luminal lipases from the digestive gland is reported for the first time. Salivary and digestive glands were the main tissuesinvolved in the synthesis and secretion of these enzymes, but plausibly the few luminally exclusive peptidases are secretedby ventrolateral pouches or epithelial unicellular glands.