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...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-09-01
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| Series: | PLoS Pathogens |
| Online Access: | https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1011647&type=printable |
| _version_ | 1797315941722226688 |
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| author | Amicha Robertson Joseph Sall Mericien Venzon Janet J Olivas Xuhui Zheng Michael Cammer Noelle Antao Chunyi Zhou Joseph C Devlin Rafaela Saes Thur Jeffrey Bethony Peter Nejsum Bo Shopsin Victor J Torres Feng-Xia Liang Ken Cadwell |
| author_facet | Amicha Robertson Joseph Sall Mericien Venzon Janet J Olivas Xuhui Zheng Michael Cammer Noelle Antao Chunyi Zhou Joseph C Devlin Rafaela Saes Thur Jeffrey Bethony Peter Nejsum Bo Shopsin Victor J Torres Feng-Xia Liang Ken Cadwell |
| author_sort | Amicha Robertson |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-03-08T03:11:10Z |
| format | Article |
| id | doaj.art-cc392483bb274eae93333f24cf78f713 |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-03-08T03:11:10Z |
| publishDate | 2023-09-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-cc392483bb274eae93333f24cf78f7132024-02-13T05:32:32ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742023-09-01199e101164710.1371/journal.ppat.1011647Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching.Amicha RobertsonJoseph SallMericien VenzonJanet J OlivasXuhui ZhengMichael CammerNoelle AntaoChunyi ZhouJoseph C DevlinRafaela Saes ThurJeffrey BethonyPeter NejsumBo ShopsinVictor J TorresFeng-Xia LiangKen CadwellThe 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.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1011647&type=printable |
| spellingShingle | Amicha Robertson Joseph Sall Mericien Venzon Janet J Olivas Xuhui Zheng Michael Cammer Noelle Antao Chunyi Zhou Joseph C Devlin Rafaela Saes Thur Jeffrey Bethony Peter Nejsum Bo Shopsin Victor J Torres Feng-Xia Liang Ken Cadwell Bacterial contact induces polar plug disintegration to mediate whipworm egg hatching. PLoS Pathogens |
| 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 |
| url | https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1011647&type=printable |
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