Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching

Amicha Robertson, Department of Microbiology, New York University Grossman School of Medicine, New York, New York, United States of America.
Joseph Sall, Microscopy Laboratory, Division of Advanced Research Technologies, New York University Langone Health, New York, New York, United States of America.
Mericien Venzon, Department of Microbiology, New York University Grossman School of Medicine, New York, New York, United States of America.
Janet J. Olivas, Department of Microbiology, New York University Grossman School of Medicine, New York, New York, United States of America.
Xuhui Zheng, Department of Microbiology, New York University Grossman School of Medicine, New York, New York, United States of America.
Michael Cammer, Microscopy Laboratory, Division of Advanced Research Technologies, New York University Langone Health, New York, New York, United States of America.
Noelle Antao, Department of Cell Biology, New York University Grossman School of Medicine, New York New York, United States of America.
Chunyi Zhou, Department of Microbiology, New York University Grossman School of Medicine, New York, New York, United States of America.
Joseph C. Devlin, Department of Microbiology, New York University Grossman School of Medicine, New York, New York, United States of America.
Rafaela Saes Thur, Department of Microbiology, Immunology and Tropical Medicine, George Washington University, Washington DC, United States of America.
Jeffrey Bethony, Department of Microbiology, Immunology and Tropical Medicine, George Washington University, Washington DC, United States of America.
Peter Nejsum, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.
Bo Shopsin, Department of Microbiology, New York University Grossman School of Medicine, New York, New York, United States of America.
Victor J. Torres, Department of Microbiology, New York University Grossman School of Medicine, New York, New York, United States of America.
Feng-Xia Liang, Microscopy Laboratory, Division of Advanced Research Technologies, New York University Langone Health, New York, New York, United States of America.
Ken Cadwell, Division of Gastroenterology and Hepatology, Department of Medicine, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, United States of America.

Document Type

Journal Article

Publication Date

9-22-2023

Journal

PLoS pathogens

Volume

19

Issue

9

DOI

10.1371/journal.ppat.1011647

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. Unrelated bacteria induced similar loss of electron density and dissolution of the structural integrity of the plugs. Egg hatching was most efficient when high densities of bacteria were bound to the poles. 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.

Department

Microbiology, Immunology, and Tropical Medicine

Link to Full Text

Share

COinS