Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching

Abstract

The bacterial microbiota promotes the life cycle of the intestine-dwelling whipworm Trichuris by mediating hatching of parasite eggs ingested by the mammalian host. Despite the enormous disease burden associated with Trichuris colonization, the mechanisms underlying this transkingdom interaction have been obscure. Here, we used a multiscale microscopy approach to define the structural events associated with bacteria-mediated hatching of eggs for the murine model parasite Trichuris muris. Through the combination of scanning electron microscopy (SEM) and serial block face SEM (SBFSEM), we visualized the outer surface morphology of the shell and generated 3D structures of the egg and larva during the hatching process. These images revealed that exposure to hatching-inducing bacteria catalyzed asymmetric degradation of the polar plugs prior to exit by the larva. Although unrelated bacteria induced similar loss of electron density and dissolution of the structural integrity of the plugs, egg hatching was most efficient in the presence of bacteria that bound poles with high density such as Staphylococcus aureus. Consistent with the ability of taxonomically distant bacteria to induce hatching, additional results suggest chitinase released from larva within the eggs degrade the plugs from the inside instead of enzymes produced by bacteria in the external environment. These findings define at ultrastructure resolution the evolutionary adaptation of a parasite for the microbe-rich environment of the mammalian gut.

Functional characterization of helminth-associated Clostridiales reveals covariates of Treg differentiation

“…Arylamidases catalyze the release of N-terminal amino acids from peptides. Recently, we discovered that protease inhibitors block bacteria-mediated egg hatching, most likely by interfering with surface protein structures necessary for contact between bacteria and egg [87]. Therefore, we speculate that valine arylamidase production is necessary for structural properties of the bacteria that mediate hatching.…”

Trichuris muris egg-hatching assay for anthelminthic drug discovery and characterization

“…We evaluated the hatching inducing potential of bacterial species found to indwell the T. muris hatching site within the small intestine ( Escherichia coli and Enterobacter hormaechei ) and with reported sufficient hatching results in comparable studies ( Staphylococcus aureus , Paraclostridium spp. and Pseudomonas aureginosa ) ( Sargsian et al, 2022 ; Robertson et al, 2023 ). We further selected S. salivarius that was previously associated with reduced drug efficacy in Trichuris trichiura infected patients ( Schneeberger et al, 2022 ), which may indicate a role of the bacterium in promoting the early life cycle of the parasite.…”

“…While hookworm larvae hatch spontaneously, embryonated Trichuris eggs ( Forman et al, 2021 ) exploit and require the presence of host microbiota to hatch and invade the host ( Hayes et al, 2010 ; Koyama, 2013 ; Lawson et al, 2021 ). Although several bacterial species have been found to induce hatching ( Hayes et al, 2010 ; Koyama, 2013 ; Wimmersberger et al, 2013 ; Lawson et al, 2021 ; Sargsian et al, 2022 ; Robertson et al, 2023 ) or modify treatment ( Schneeberger et al, 2022 ), the ideal conditions for hatching remain uncertain, resulting in highly variable hatching yields and difficulties to compare results between laboratories.…”

Mucin-degrading gut bacteria promote anti-parasitic immunity

“…Since they occupy the same host environment, it is no surprise that enteric parasites such as helminths strongly interact with the gut microbiome 5,6 . Although these interactions may lead to the suppression of either the gut microbiome or the helminth [5][6][7] , in case of T. muris, bacterial-helminth crosstalk is essential for worm hatching, as the parasite eggs fail to hatch and establish in germ-free environments [8][9][10] . Once the worm has settled in the intestinal epithelium, the bacterial-helminth dynamics appear mainly unidirectional, with helminths altering the microbiome composition through various mechanisms, including through helminth excretory-secretory products or host anti-microbial peptides, released in response to the parasite [11][12][13][14][15] .…”