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Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching

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 hav...

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Autores principales: Robertson, Amicha, Sall, Joseph, Venzon, Mericien, Olivas, Janet J., Zheng, Xuhui, Cammer, Michael, Antao, Noelle, Zhou, Chunyi, Devlin, Joseph C., Saes Thur, Rafaela, Bethony, Jeffrey, Nejsum, Peter, Shopsin, Bo, Torres, Victor J., Liang, Feng-Xia, Cadwell, Ken
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10550136/
https://www.ncbi.nlm.nih.gov/pubmed/37738244
http://dx.doi.org/10.1371/journal.ppat.1011647
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author Robertson, Amicha
Sall, Joseph
Venzon, Mericien
Olivas, Janet J.
Zheng, Xuhui
Cammer, Michael
Antao, Noelle
Zhou, Chunyi
Devlin, Joseph C.
Saes Thur, Rafaela
Bethony, Jeffrey
Nejsum, Peter
Shopsin, Bo
Torres, Victor J.
Liang, Feng-Xia
Cadwell, Ken
author_facet Robertson, Amicha
Sall, Joseph
Venzon, Mericien
Olivas, Janet J.
Zheng, Xuhui
Cammer, Michael
Antao, Noelle
Zhou, Chunyi
Devlin, Joseph C.
Saes Thur, Rafaela
Bethony, Jeffrey
Nejsum, Peter
Shopsin, Bo
Torres, Victor J.
Liang, Feng-Xia
Cadwell, Ken
author_sort Robertson, Amicha
collection PubMed
description 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.
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spelling pubmed-105501362023-10-05 Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching Robertson, Amicha Sall, Joseph Venzon, Mericien Olivas, Janet J. Zheng, Xuhui Cammer, Michael Antao, Noelle Zhou, Chunyi Devlin, Joseph C. Saes Thur, Rafaela Bethony, Jeffrey Nejsum, Peter Shopsin, Bo Torres, Victor J. Liang, Feng-Xia Cadwell, Ken PLoS Pathog Research Article 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. Public Library of Science 2023-09-22 /pmc/articles/PMC10550136/ /pubmed/37738244 http://dx.doi.org/10.1371/journal.ppat.1011647 Text en © 2023 Robertson et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Robertson, Amicha
Sall, Joseph
Venzon, Mericien
Olivas, Janet J.
Zheng, Xuhui
Cammer, Michael
Antao, Noelle
Zhou, Chunyi
Devlin, Joseph C.
Saes Thur, Rafaela
Bethony, Jeffrey
Nejsum, Peter
Shopsin, Bo
Torres, Victor J.
Liang, Feng-Xia
Cadwell, Ken
Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching
title Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching
title_full Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching
title_fullStr Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching
title_full_unstemmed Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching
title_short Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching
title_sort bacterial contact induces polar plug disintegration to mediate whipworm egg hatching
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10550136/
https://www.ncbi.nlm.nih.gov/pubmed/37738244
http://dx.doi.org/10.1371/journal.ppat.1011647
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