Transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infection
Termites are social insects that live in the soil or in decaying wood, where exposure to pathogens should be common. However, these pathogens rarely cause mortality in established colonies. In addition to social immunity, the gut symbionts of termites are expected to assist in protecting their hosts...
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| Format: | Article |
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Frontiers Media S.A.
2023-04-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphys.2023.1194370/full |
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| author | Ya-ling Tang Ya-ling Tang Yun-hui Kong Sheng Qin Sheng Qin Austin Merchant Ji-zhe Shi Xu-guo Zhou Mu-wang Li Mu-wang Li Qian Wang |
| author_facet | Ya-ling Tang Ya-ling Tang Yun-hui Kong Sheng Qin Sheng Qin Austin Merchant Ji-zhe Shi Xu-guo Zhou Mu-wang Li Mu-wang Li Qian Wang |
| author_sort | Ya-ling Tang |
| collection | DOAJ |
| description | Termites are social insects that live in the soil or in decaying wood, where exposure to pathogens should be common. However, these pathogens rarely cause mortality in established colonies. In addition to social immunity, the gut symbionts of termites are expected to assist in protecting their hosts, though the specific contributions are unclear. In this study, we examined this hypothesis in Odontotermes formosanus, a fungus-growing termite in the family Termitidae, by 1) disrupting its gut microbiota with the antibiotic kanamycin, 2) challenging O. formosanus with the entomopathogenic fungus Metarhizium robertsii, and finally 3) sequencing the resultant gut transcriptomes. As a result, 142531 transcripts and 73608 unigenes were obtained, and unigenes were annotated following NR, NT, KO, Swiss-Prot, PFAM, GO, and KOG databases. Among them, a total of 3,814 differentially expressed genes (DEGs) were identified between M. robertsii infected termites with or without antibiotics treatment. Given the lack of annotated genes in O. formosanus transcriptomes, we examined the expression profiles of the top 20 most significantly differentially expressed genes using qRT-PCR. Several of these genes, including APOA2, Calpain-5, and Hsp70, were downregulated in termites exposed to both antibiotics and pathogen but upregulated in those exposed only to the pathogen, suggesting that gut microbiota might buffer/facilitate their hosts against infection by finetuning physiological and biochemical processes, including innate immunity, protein folding, and ATP synthesis. Overall, our combined results imply that stabilization of gut microbiota can assist termites in maintaining physiological and biochemical homeostasis when foreign pathogenic fungi invade. |
| first_indexed | 2024-03-13T11:02:50Z |
| format | Article |
| id | doaj.art-d25a95fd51f54969bf37bce830f0b126 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-03-13T11:02:50Z |
| publishDate | 2023-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-d25a95fd51f54969bf37bce830f0b1262023-05-16T16:10:31ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2023-04-011410.3389/fphys.2023.11943701194370Transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infectionYa-ling Tang0Ya-ling Tang1Yun-hui Kong2Sheng Qin3Sheng Qin4Austin Merchant5Ji-zhe Shi6Xu-guo Zhou7Mu-wang Li8Mu-wang Li9Qian Wang10Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, ChinaShanghai First Maternity and Infant Hospital, Tongji University School of Medicine, Shanghai, ChinaJiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, ChinaJiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, ChinaKey Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Research Institute, Chinese Academy of Agricultural Science, Zhenjiang, Jiangsu Province, ChinaDepartment of Entomology, University of Kentucky, Lexington, KY, United StatesDepartment of Entomology, University of Kentucky, Lexington, KY, United StatesDepartment of Entomology, University of Kentucky, Lexington, KY, United StatesJiangsu Key Laboratory of Sericultural Biology and Biotechnology, School of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu Province, ChinaKey Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericultural Research Institute, Chinese Academy of Agricultural Science, Zhenjiang, Jiangsu Province, ChinaShanghai First Maternity and Infant Hospital, Tongji University School of Medicine, Shanghai, ChinaTermites are social insects that live in the soil or in decaying wood, where exposure to pathogens should be common. However, these pathogens rarely cause mortality in established colonies. In addition to social immunity, the gut symbionts of termites are expected to assist in protecting their hosts, though the specific contributions are unclear. In this study, we examined this hypothesis in Odontotermes formosanus, a fungus-growing termite in the family Termitidae, by 1) disrupting its gut microbiota with the antibiotic kanamycin, 2) challenging O. formosanus with the entomopathogenic fungus Metarhizium robertsii, and finally 3) sequencing the resultant gut transcriptomes. As a result, 142531 transcripts and 73608 unigenes were obtained, and unigenes were annotated following NR, NT, KO, Swiss-Prot, PFAM, GO, and KOG databases. Among them, a total of 3,814 differentially expressed genes (DEGs) were identified between M. robertsii infected termites with or without antibiotics treatment. Given the lack of annotated genes in O. formosanus transcriptomes, we examined the expression profiles of the top 20 most significantly differentially expressed genes using qRT-PCR. Several of these genes, including APOA2, Calpain-5, and Hsp70, were downregulated in termites exposed to both antibiotics and pathogen but upregulated in those exposed only to the pathogen, suggesting that gut microbiota might buffer/facilitate their hosts against infection by finetuning physiological and biochemical processes, including innate immunity, protein folding, and ATP synthesis. Overall, our combined results imply that stabilization of gut microbiota can assist termites in maintaining physiological and biochemical homeostasis when foreign pathogenic fungi invade.https://www.frontiersin.org/articles/10.3389/fphys.2023.1194370/fulltermiteodontotermes formosanusmetarhizium robertsiide novo assemblyinnate immunitygut microbiota |
| spellingShingle | Ya-ling Tang Ya-ling Tang Yun-hui Kong Sheng Qin Sheng Qin Austin Merchant Ji-zhe Shi Xu-guo Zhou Mu-wang Li Mu-wang Li Qian Wang Transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infection Frontiers in Physiology termite odontotermes formosanus metarhizium robertsii de novo assembly innate immunity gut microbiota |
| title | Transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infection |
| title_full | Transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infection |
| title_fullStr | Transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infection |
| title_full_unstemmed | Transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infection |
| title_short | Transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infection |
| title_sort | transcriptomic dissection of termite gut microbiota following entomopathogenic fungal infection |
| topic | termite odontotermes formosanus metarhizium robertsii de novo assembly innate immunity gut microbiota |
| url | https://www.frontiersin.org/articles/10.3389/fphys.2023.1194370/full |
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