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Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis

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...

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Autores principales: Ren, Xueming, Cao, Shuai, Akami, Mazarin, Mansour, Abdelaziz, Yang, Yishi, Jiang, Nan, Wang, Haoran, Zhang, Guijian, Qi, Xuewei, Xu, Penghui, Guo, Tong, Niu, Changying
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9476588/
https://www.ncbi.nlm.nih.gov/pubmed/36104720
http://dx.doi.org/10.1186/s12915-022-01399-9
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author Ren, Xueming
Cao, Shuai
Akami, Mazarin
Mansour, Abdelaziz
Yang, Yishi
Jiang, Nan
Wang, Haoran
Zhang, Guijian
Qi, Xuewei
Xu, Penghui
Guo, Tong
Niu, Changying
author_facet Ren, Xueming
Cao, Shuai
Akami, Mazarin
Mansour, Abdelaziz
Yang, Yishi
Jiang, Nan
Wang, Haoran
Zhang, Guijian
Qi, Xuewei
Xu, Penghui
Guo, Tong
Niu, Changying
author_sort Ren, Xueming
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01399-9.
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spelling pubmed-94765882022-09-16 Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis Ren, Xueming Cao, Shuai Akami, Mazarin Mansour, Abdelaziz Yang, Yishi Jiang, Nan Wang, Haoran Zhang, Guijian Qi, Xuewei Xu, Penghui Guo, Tong Niu, Changying BMC Biol Research Article 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01399-9. BioMed Central 2022-09-14 /pmc/articles/PMC9476588/ /pubmed/36104720 http://dx.doi.org/10.1186/s12915-022-01399-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Ren, Xueming
Cao, Shuai
Akami, Mazarin
Mansour, Abdelaziz
Yang, Yishi
Jiang, Nan
Wang, Haoran
Zhang, Guijian
Qi, Xuewei
Xu, Penghui
Guo, Tong
Niu, Changying
Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis
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 Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9476588/
https://www.ncbi.nlm.nih.gov/pubmed/36104720
http://dx.doi.org/10.1186/s12915-022-01399-9
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