Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis
Abstract Background Nitrogen is considered the most limiting nutrient element for herbivorous insects. To alleviate nitrogen limitation, insects have evolved various symbiotically mediated strategies that enable them to colonize nitrogen-poor habitats or exploit nitrogen-poor diets. In frugivorous t...
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BMC
2022-09-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01399-9 |
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| author | Xueming Ren Shuai Cao Mazarin Akami Abdelaziz Mansour Yishi Yang Nan Jiang Haoran Wang Guijian Zhang Xuewei Qi Penghui Xu Tong Guo Changying Niu |
| author_facet | Xueming Ren Shuai Cao Mazarin Akami Abdelaziz Mansour Yishi Yang Nan Jiang Haoran Wang Guijian Zhang Xuewei Qi Penghui Xu Tong Guo Changying Niu |
| author_sort | Xueming Ren |
| collection | DOAJ |
| description | Abstract Background Nitrogen is considered the most limiting nutrient element for herbivorous insects. To alleviate nitrogen limitation, insects have evolved various symbiotically mediated strategies that enable them to colonize nitrogen-poor habitats or exploit nitrogen-poor diets. In frugivorous tephritid larvae developing in fruit pulp under nitrogen stress, it remains largely unknown how nitrogen is obtained and larval development is completed. Results In this study, we used metagenomics and metatranscriptomics sequencing technologies as well as in vitro verification tests to uncover the mechanism underlying the nitrogen exploitation in the larvae of Bactrocera dorsalis. Our results showed that nitrogenous waste recycling (NWR) could be successfully driven by symbiotic bacteria, including Enterobacterales, Lactobacillales, Orbales, Pseudomonadales, Flavobacteriales, and Bacteroidales. In this process, urea hydrolysis in the larval gut was mainly mediated by Morganella morganii and Klebsiella oxytoca. In addition, core bacteria mediated essential amino acid (arginine excluded) biosynthesis by ammonium assimilation and transamination. Conclusions Symbiotic bacteria contribute to nitrogen transformation in the larvae of B. dorsalis in fruit pulp. Our findings suggest that the pattern of NWR is more likely to be applied by B. dorsalis, and M. morganii, K. oxytoca, and other urease-positive strains play vital roles in hydrolysing nitrogenous waste and providing metabolizable nitrogen for B. dorsalis. |
| first_indexed | 2024-04-11T09:54:31Z |
| format | Article |
| id | doaj.art-e0ea7a3640a145d983c6932aff047de9 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-11T09:54:31Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-e0ea7a3640a145d983c6932aff047de92022-12-22T04:30:42ZengBMCBMC Biology1741-70072022-09-0120111610.1186/s12915-022-01399-9Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalisXueming Ren0Shuai Cao1Mazarin Akami2Abdelaziz Mansour3Yishi Yang4Nan Jiang5Haoran Wang6Guijian Zhang7Xuewei Qi8Penghui Xu9Tong Guo10Changying Niu11Hubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityHubei Key Laboratory of Insect Resource Application and Sustainable Pest Control, College of Plant Science & Technology, Huazhong Agricultural UniversityAbstract Background Nitrogen is considered the most limiting nutrient element for herbivorous insects. To alleviate nitrogen limitation, insects have evolved various symbiotically mediated strategies that enable them to colonize nitrogen-poor habitats or exploit nitrogen-poor diets. In frugivorous tephritid larvae developing in fruit pulp under nitrogen stress, it remains largely unknown how nitrogen is obtained and larval development is completed. Results In this study, we used metagenomics and metatranscriptomics sequencing technologies as well as in vitro verification tests to uncover the mechanism underlying the nitrogen exploitation in the larvae of Bactrocera dorsalis. Our results showed that nitrogenous waste recycling (NWR) could be successfully driven by symbiotic bacteria, including Enterobacterales, Lactobacillales, Orbales, Pseudomonadales, Flavobacteriales, and Bacteroidales. In this process, urea hydrolysis in the larval gut was mainly mediated by Morganella morganii and Klebsiella oxytoca. In addition, core bacteria mediated essential amino acid (arginine excluded) biosynthesis by ammonium assimilation and transamination. Conclusions Symbiotic bacteria contribute to nitrogen transformation in the larvae of B. dorsalis in fruit pulp. Our findings suggest that the pattern of NWR is more likely to be applied by B. dorsalis, and M. morganii, K. oxytoca, and other urease-positive strains play vital roles in hydrolysing nitrogenous waste and providing metabolizable nitrogen for B. dorsalis.https://doi.org/10.1186/s12915-022-01399-9Bactrocera dorsalisNitrogenous waste recyclingBiological nitrogen fixationAmino acid biosynthesisUrease activity |
| spellingShingle | Xueming Ren Shuai Cao Mazarin Akami Abdelaziz Mansour Yishi Yang Nan Jiang Haoran Wang Guijian Zhang Xuewei Qi Penghui Xu Tong Guo Changying Niu Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis BMC Biology Bactrocera dorsalis Nitrogenous waste recycling Biological nitrogen fixation Amino acid biosynthesis Urease activity |
| title | Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis |
| title_full | Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis |
| title_fullStr | Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis |
| title_full_unstemmed | Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis |
| title_short | Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis |
| title_sort | gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly bactrocera dorsalis |
| topic | Bactrocera dorsalis Nitrogenous waste recycling Biological nitrogen fixation Amino acid biosynthesis Urease activity |
| url | https://doi.org/10.1186/s12915-022-01399-9 |
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