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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, Thur, Rafaela Saes, Bethony, Jeffrey, Nejsum, Peter, Torres, Victor J., Liang, Feng-Xia, Cadwell, Ken
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10054943/
https://www.ncbi.nlm.nih.gov/pubmed/36993552
http://dx.doi.org/10.1101/2023.03.13.532458
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author Robertson, Amicha
Sall, Joseph
Venzon, Mericien
Olivas, Janet J.
Zheng, Xuhui
Cammer, Michael
Antao, Noelle
Thur, Rafaela Saes
Bethony, Jeffrey
Nejsum, Peter
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
Thur, Rafaela Saes
Bethony, Jeffrey
Nejsum, Peter
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. 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.
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spelling pubmed-100549432023-03-30 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 Thur, Rafaela Saes Bethony, Jeffrey Nejsum, Peter Torres, Victor J. Liang, Feng-Xia Cadwell, Ken bioRxiv 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. 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. Cold Spring Harbor Laboratory 2023-03-13 /pmc/articles/PMC10054943/ /pubmed/36993552 http://dx.doi.org/10.1101/2023.03.13.532458 Text en https://creativecommons.org/licenses/by-nd/4.0/This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, and only so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Robertson, Amicha
Sall, Joseph
Venzon, Mericien
Olivas, Janet J.
Zheng, Xuhui
Cammer, Michael
Antao, Noelle
Thur, Rafaela Saes
Bethony, Jeffrey
Nejsum, Peter
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 Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10054943/
https://www.ncbi.nlm.nih.gov/pubmed/36993552
http://dx.doi.org/10.1101/2023.03.13.532458
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