Hatching of whipworm eggs induced by bacterial contact is serine-protease dependent.
Whipworms (Trichuris spp) are ubiquitous parasites of humans and domestic and wild mammals that cause chronic disease, considerably impacting human and animal health. Egg hatching is a critical phase in the whipworm life cycle that marks the initiation of infection, with newly hatched larvae rapidly...
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2025-01-01
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| Series: | PLoS Pathogens |
| Online Access: | https://doi.org/10.1371/journal.ppat.1012502 |
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| author | David Goulding Charlotte Tolley Tapoka T Mkandawire Stephen R Doyle Emily Hart Paul M Airs Richard K Grencis Matthew Berriman María A Duque-Correa |
| author_facet | David Goulding Charlotte Tolley Tapoka T Mkandawire Stephen R Doyle Emily Hart Paul M Airs Richard K Grencis Matthew Berriman María A Duque-Correa |
| author_sort | David Goulding |
| collection | DOAJ |
| description | Whipworms (Trichuris spp) are ubiquitous parasites of humans and domestic and wild mammals that cause chronic disease, considerably impacting human and animal health. Egg hatching is a critical phase in the whipworm life cycle that marks the initiation of infection, with newly hatched larvae rapidly migrating to and invading host intestinal epithelial cells. Hatching is triggered by the host microbiota; however, the physical and chemical interactions between bacteria and whipworm eggs, as well as the bacterial and larval responses that result in the disintegration of the polar plug and larval eclosion, are not completely understood. Here, we examined hatching in the murine whipworm, Trichuris muris, and investigated the role of specific bacterial and larval structures and molecules in this process. Using scanning and transmission electron microscopy, we characterised the physical interactions of both fimbriated (Escherichia coli, Salmonella typhimurium and Pseudomonas aeruginosa) and non-fimbriated (Staphylococcus aureus) bacteria with the egg polar plugs during the induction/initiation stage, and visualised the effects of structural changes in the polar plugs, leading to larval eclosion. Further, we found that protease inhibitors blocked whipworm hatching induced by both fimbriated and non-fimbriated bacteria in a dose-dependent manner, suggesting the partial involvement of bacterial enzymes in this process. In addition, we identified the minimal egg developmental timing required for whipworm hatching, and transcriptomic analysis of T. muris eggs through embryonation revealed the specific upregulation of serine proteases (S01A family) in fully embryonated eggs containing 'hatch-ready' L1 larvae. Finally, we demonstrated that inhibition of serine proteases with the serine-protease inhibitor Pefabloc ablated T. muris egg hatching induced by bacteria. Collectively, our findings unravel the temporal and physicochemical bacterial-egg interactions leading to whipworm hatching and indicate serine proteases of both bacterial and larval origin mediate these processes. |
| format | Article |
| id | doaj-art-c38bdd80d27745bdae12d70c9ed83570 |
| institution | OA Journals |
| issn | 1553-7366 1553-7374 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj-art-c38bdd80d27745bdae12d70c9ed835702025-08-20T02:31:38ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-01-01211e101250210.1371/journal.ppat.1012502Hatching of whipworm eggs induced by bacterial contact is serine-protease dependent.David GouldingCharlotte TolleyTapoka T MkandawireStephen R DoyleEmily HartPaul M AirsRichard K GrencisMatthew BerrimanMaría A Duque-CorreaWhipworms (Trichuris spp) are ubiquitous parasites of humans and domestic and wild mammals that cause chronic disease, considerably impacting human and animal health. Egg hatching is a critical phase in the whipworm life cycle that marks the initiation of infection, with newly hatched larvae rapidly migrating to and invading host intestinal epithelial cells. Hatching is triggered by the host microbiota; however, the physical and chemical interactions between bacteria and whipworm eggs, as well as the bacterial and larval responses that result in the disintegration of the polar plug and larval eclosion, are not completely understood. Here, we examined hatching in the murine whipworm, Trichuris muris, and investigated the role of specific bacterial and larval structures and molecules in this process. Using scanning and transmission electron microscopy, we characterised the physical interactions of both fimbriated (Escherichia coli, Salmonella typhimurium and Pseudomonas aeruginosa) and non-fimbriated (Staphylococcus aureus) bacteria with the egg polar plugs during the induction/initiation stage, and visualised the effects of structural changes in the polar plugs, leading to larval eclosion. Further, we found that protease inhibitors blocked whipworm hatching induced by both fimbriated and non-fimbriated bacteria in a dose-dependent manner, suggesting the partial involvement of bacterial enzymes in this process. In addition, we identified the minimal egg developmental timing required for whipworm hatching, and transcriptomic analysis of T. muris eggs through embryonation revealed the specific upregulation of serine proteases (S01A family) in fully embryonated eggs containing 'hatch-ready' L1 larvae. Finally, we demonstrated that inhibition of serine proteases with the serine-protease inhibitor Pefabloc ablated T. muris egg hatching induced by bacteria. Collectively, our findings unravel the temporal and physicochemical bacterial-egg interactions leading to whipworm hatching and indicate serine proteases of both bacterial and larval origin mediate these processes.https://doi.org/10.1371/journal.ppat.1012502 |
| spellingShingle | David Goulding Charlotte Tolley Tapoka T Mkandawire Stephen R Doyle Emily Hart Paul M Airs Richard K Grencis Matthew Berriman María A Duque-Correa Hatching of whipworm eggs induced by bacterial contact is serine-protease dependent. PLoS Pathogens |
| title | Hatching of whipworm eggs induced by bacterial contact is serine-protease dependent. |
| title_full | Hatching of whipworm eggs induced by bacterial contact is serine-protease dependent. |
| title_fullStr | Hatching of whipworm eggs induced by bacterial contact is serine-protease dependent. |
| title_full_unstemmed | Hatching of whipworm eggs induced by bacterial contact is serine-protease dependent. |
| title_short | Hatching of whipworm eggs induced by bacterial contact is serine-protease dependent. |
| title_sort | hatching of whipworm eggs induced by bacterial contact is serine protease dependent |
| url | https://doi.org/10.1371/journal.ppat.1012502 |
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