Digestive exophagy of bacterial biofilms by the amoeba Entamoeba histolytica and its impact on virulence and stress tolerance
2The Robert H. Smith Faculty of Agriculture, Food & Environment, The Hebrew University of Jerusalem, Israel
The human protozoan parasite Entamoeba histolytica is responsible for amebiasis, a disease endemic to developing countries. E. histolytica trophozoites are released from the cysts to colonize the large intestine, where they primarily feed on bacterial cells. In these scenarios, bacterial cells are residing in aggregates or structured communities too large for phagocytosis.
Our results show that E. histolytica can degrade pre-established community biofilms of Bacillus subtilis and Escherichia coli in a dose- and time-dependent manner. Surprisingly, trophozoites incubated with B. subtilis biofilms exhibit a unique transcriptome compared to those incubated with planktonic cells or without bacteria. The specific recognition of biofilm by the parasite includes the induction of cysteine proteases (CPs). In agreement, inhibiting CPs by E64D or specific sRNA impairs the degradation of biofilms. The extracellular matrix protein TasA serves as a substrate to the predator CPs and as the ligand for E. histolytica adhesion. The partial biofilm digestion leads to the activation of the stress response in the overall community of B. subtilis cells.
The interaction with B. subtilis biofilms is also associated with lower expression levels of oxidoreductases by the predator, which can be a readout of the embedding of trophozoites within the bacterial extracellular matrix.
Our results indicate that parasites may digest biofilm cells by a controlled mechanism of digestive exophagy and that activating digestive enzymes is a conserved mechanism for biofilm degradation. Furthermore, the partially digested biofilms can serve as an unexpected shield protecting parasites from oxidative environments, thereby regulating the parasite`s persistence and virulence.