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Background  The endoglycosidase heparanase which degrades heparan sulfate proteoglycans, exerts a pro-inflammatory mediator in various inflammatory disorders. However, the function and underlying mechanism of heparanase in acute pancreatitis remain poorly understood. Here, we investigated the interplay between heparanase and the gut microbiota in the development of acute pancreatitis.    Methods  Acute pancreatitis was induced in wild-type and heparanase-transgenic mice by administration of caerulein. The differences in gut microbiota were analyzed by 16S ribosomal RNA sequencing. Antibiotic cocktail experiment, fecal microbiota transplantation, and cohousing experiments were used to assess the role of gut microbiota.    Results  As compared with wild-type mice, acute pancreatitis was exacerbated in heparanase-transgenic mice. Moreover, the gut microbiota differed between heparanase-transgenic and wild-type mice. Heparanase exacerbated acute pancreatitis in a gut microbiota-dependent manner. Specially, the commensal  Parabacteroid es contributed most to distinguish the differences between wild-type and heparanase-transgenic mice. Administration of  Parabacteroides  alleviated acute pancreatitis in wild-type and heparanase-transgenic mice. In addition,  Parabacteroides  produced acetate to alleviate heparanase-exacerbated acute pancreatitis through reducing neutrophil infiltration.    Conclusions  The gut–pancreas axis played an important role in the development of acute pancreatitis and the acetate produced by  Parabacteroides  may be beneficial for acute pancreatitis treatment.Video abstractSupplementary Information  The online version contains supplementary material available at 10.1186/s40168-021-01065-2.

Parabacteroides produces acetate to alleviate heparanase-exacerbated acute pancreatitis through reducing neutrophil infiltration