Key processes required for the different stages of fungal carnivory by a nematode-trapping fungus.
Nutritional deprivation triggers a switch from a saprotrophic to predatory lifestyle in soil-dwelling nematode-trapping fungi (NTF). In particular, the NTF Arthrobotrys oligospora secretes food and sex cues to lure nematodes to its mycelium and is triggered to develop specialized trapping devices. C...
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Public Library of Science (PLoS)
2023-11-01
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| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002400&type=printable |
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| author | Hung-Che Lin Guillermo Vidal-Diez de Ulzurrun Sheng-An Chen Ching-Ting Yang Rebecca J Tay Tomoyo Iizuka Tsung-Yu Huang Chih-Yen Kuo A Pedro Gonçalves Siou-Ying Lin Yu-Chu Chang Jason E Stajich Erich M Schwarz Yen-Ping Hsueh |
| author_facet | Hung-Che Lin Guillermo Vidal-Diez de Ulzurrun Sheng-An Chen Ching-Ting Yang Rebecca J Tay Tomoyo Iizuka Tsung-Yu Huang Chih-Yen Kuo A Pedro Gonçalves Siou-Ying Lin Yu-Chu Chang Jason E Stajich Erich M Schwarz Yen-Ping Hsueh |
| author_sort | Hung-Che Lin |
| collection | DOAJ |
| description | Nutritional deprivation triggers a switch from a saprotrophic to predatory lifestyle in soil-dwelling nematode-trapping fungi (NTF). In particular, the NTF Arthrobotrys oligospora secretes food and sex cues to lure nematodes to its mycelium and is triggered to develop specialized trapping devices. Captured nematodes are then invaded and digested by the fungus, thus serving as a food source. In this study, we examined the transcriptomic response of A. oligospora across the stages of sensing, trap development, and digestion upon exposure to the model nematode Caenorhabditis elegans. A. oligospora enacts a dynamic transcriptomic response, especially of protein secretion-related genes, in the presence of prey. Two-thirds of the predicted secretome of A. oligospora was up-regulated in the presence of C. elegans at all time points examined, and among these secreted proteins, 38.5% are predicted to be effector proteins. Furthermore, functional studies disrupting the t-SNARE protein Sso2 resulted in impaired ability to capture nematodes. Additionally, genes of the DUF3129 family, which are expanded in the genomes of several NTF, were highly up-regulated upon nematode exposure. We observed the accumulation of highly expressed DUF3129 proteins in trap cells, leading us to name members of this gene family as Trap Enriched Proteins (TEPs). Gene deletion of the most highly expressed TEP gene, TEP1, impairs the function of traps and prevents the fungus from capturing prey efficiently. In late stages of predation, we observed up-regulation of a variety of proteases, including metalloproteases. Following penetration of nematodes, these metalloproteases facilitate hyphal growth required for colonization of prey. These findings provide insights into the biology of the predatory lifestyle switch in a carnivorous fungus and provide frameworks for other fungal-nematode predator-prey systems. |
| format | Article |
| id | doaj-art-8072095ca33242eb9838f5838f5bbd0b |
| institution | Kabale University |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2023-11-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-8072095ca33242eb9838f5838f5bbd0b2025-08-20T03:29:03ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-11-012111e300240010.1371/journal.pbio.3002400Key processes required for the different stages of fungal carnivory by a nematode-trapping fungus.Hung-Che LinGuillermo Vidal-Diez de UlzurrunSheng-An ChenChing-Ting YangRebecca J TayTomoyo IizukaTsung-Yu HuangChih-Yen KuoA Pedro GonçalvesSiou-Ying LinYu-Chu ChangJason E StajichErich M SchwarzYen-Ping HsuehNutritional deprivation triggers a switch from a saprotrophic to predatory lifestyle in soil-dwelling nematode-trapping fungi (NTF). In particular, the NTF Arthrobotrys oligospora secretes food and sex cues to lure nematodes to its mycelium and is triggered to develop specialized trapping devices. Captured nematodes are then invaded and digested by the fungus, thus serving as a food source. In this study, we examined the transcriptomic response of A. oligospora across the stages of sensing, trap development, and digestion upon exposure to the model nematode Caenorhabditis elegans. A. oligospora enacts a dynamic transcriptomic response, especially of protein secretion-related genes, in the presence of prey. Two-thirds of the predicted secretome of A. oligospora was up-regulated in the presence of C. elegans at all time points examined, and among these secreted proteins, 38.5% are predicted to be effector proteins. Furthermore, functional studies disrupting the t-SNARE protein Sso2 resulted in impaired ability to capture nematodes. Additionally, genes of the DUF3129 family, which are expanded in the genomes of several NTF, were highly up-regulated upon nematode exposure. We observed the accumulation of highly expressed DUF3129 proteins in trap cells, leading us to name members of this gene family as Trap Enriched Proteins (TEPs). Gene deletion of the most highly expressed TEP gene, TEP1, impairs the function of traps and prevents the fungus from capturing prey efficiently. In late stages of predation, we observed up-regulation of a variety of proteases, including metalloproteases. Following penetration of nematodes, these metalloproteases facilitate hyphal growth required for colonization of prey. These findings provide insights into the biology of the predatory lifestyle switch in a carnivorous fungus and provide frameworks for other fungal-nematode predator-prey systems.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002400&type=printable |
| spellingShingle | Hung-Che Lin Guillermo Vidal-Diez de Ulzurrun Sheng-An Chen Ching-Ting Yang Rebecca J Tay Tomoyo Iizuka Tsung-Yu Huang Chih-Yen Kuo A Pedro Gonçalves Siou-Ying Lin Yu-Chu Chang Jason E Stajich Erich M Schwarz Yen-Ping Hsueh Key processes required for the different stages of fungal carnivory by a nematode-trapping fungus. PLoS Biology |
| title | Key processes required for the different stages of fungal carnivory by a nematode-trapping fungus. |
| title_full | Key processes required for the different stages of fungal carnivory by a nematode-trapping fungus. |
| title_fullStr | Key processes required for the different stages of fungal carnivory by a nematode-trapping fungus. |
| title_full_unstemmed | Key processes required for the different stages of fungal carnivory by a nematode-trapping fungus. |
| title_short | Key processes required for the different stages of fungal carnivory by a nematode-trapping fungus. |
| title_sort | key processes required for the different stages of fungal carnivory by a nematode trapping fungus |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3002400&type=printable |
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