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Combined metagenomic and metabolomic analyses reveal that Bt rice planting alters soil C-N metabolism

The environmental impacts of genetically modified (GM) plants remain a controversial global issue. To address these issues, comprehensive environmental risk assessments of GM plants is critical for the sustainable development and application of transgenic technology. In this paper, significant diffe...

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Autores principales: Li, Peng, Ye, Shuifeng, Chen, Jun, Wang, Luyao, Li, Yujie, Ge, Lei, Wu, Guogan, Song, Lili, Wang, Cui, Sun, Yu, Wang, Jinbin, Pan, Aihu, Quan, Zhexue, Wu, Yunfei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9870860/
https://www.ncbi.nlm.nih.gov/pubmed/36690796
http://dx.doi.org/10.1038/s43705-023-00217-9
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author Li, Peng
Ye, Shuifeng
Chen, Jun
Wang, Luyao
Li, Yujie
Ge, Lei
Wu, Guogan
Song, Lili
Wang, Cui
Sun, Yu
Wang, Jinbin
Pan, Aihu
Quan, Zhexue
Wu, Yunfei
author_facet Li, Peng
Ye, Shuifeng
Chen, Jun
Wang, Luyao
Li, Yujie
Ge, Lei
Wu, Guogan
Song, Lili
Wang, Cui
Sun, Yu
Wang, Jinbin
Pan, Aihu
Quan, Zhexue
Wu, Yunfei
author_sort Li, Peng
collection PubMed
description The environmental impacts of genetically modified (GM) plants remain a controversial global issue. To address these issues, comprehensive environmental risk assessments of GM plants is critical for the sustainable development and application of transgenic technology. In this paper, significant differences were not observed between microbial metagenomic and metabolomic profiles in surface waters of the Bt rice (T1C-1, the transgenic line) and non-Bt cultivars (Minghui 63 (the isogenic line) and Zhonghua 11 (the conventional japonica cultivar)). In contrast, differences in these profiles were apparent in the rhizospheres. T1C-1 planting increased soil microbiome diversity and network stability, but did not significantly alter the abundances of potential probiotic or phytopathogenic microorganisms compared with Minghui 63 and Zhonghua 11, which revealed no adverse effects of T1C-1 on soil microbial communities. T1C-1 planting could significantly alter soil C and N, probably via the regulation of the abundances of enzymes related to soil C and N cycling. In addition, integrated multi-omic analysis of root exudate metabolomes and soil microbiomes showed that the abundances of various metabolites released as root exudates were significantly correlated with subsets of microbial populations including the Acidobacteria, Actinobacteria, Chloroflexi, and Gemmatimonadetes that were differentially abundant in T1C-1 and Mnghui 63 soils. Finally, the potential for T1C-1-associated root metabolites to exert growth effects on T1C-1-associated species was experimentally validated by analysis of bacterial cultures, revealing that Bt rice planting could selectively modulate specific root microbiota. Overall, this study indicate that Bt rice can directly modulate rhizosphere microbiome assemblages by altering the metabolic compositions of root exudates that then alters soil metabolite profiles and physiochemical properties. This study unveils the mechanistic associations of Bt plant-microorganism-environment, which provides comprehensive insights into the potential ecological impacts of GM plants.
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spelling pubmed-98708602023-01-25 Combined metagenomic and metabolomic analyses reveal that Bt rice planting alters soil C-N metabolism Li, Peng Ye, Shuifeng Chen, Jun Wang, Luyao Li, Yujie Ge, Lei Wu, Guogan Song, Lili Wang, Cui Sun, Yu Wang, Jinbin Pan, Aihu Quan, Zhexue Wu, Yunfei ISME Commun Article The environmental impacts of genetically modified (GM) plants remain a controversial global issue. To address these issues, comprehensive environmental risk assessments of GM plants is critical for the sustainable development and application of transgenic technology. In this paper, significant differences were not observed between microbial metagenomic and metabolomic profiles in surface waters of the Bt rice (T1C-1, the transgenic line) and non-Bt cultivars (Minghui 63 (the isogenic line) and Zhonghua 11 (the conventional japonica cultivar)). In contrast, differences in these profiles were apparent in the rhizospheres. T1C-1 planting increased soil microbiome diversity and network stability, but did not significantly alter the abundances of potential probiotic or phytopathogenic microorganisms compared with Minghui 63 and Zhonghua 11, which revealed no adverse effects of T1C-1 on soil microbial communities. T1C-1 planting could significantly alter soil C and N, probably via the regulation of the abundances of enzymes related to soil C and N cycling. In addition, integrated multi-omic analysis of root exudate metabolomes and soil microbiomes showed that the abundances of various metabolites released as root exudates were significantly correlated with subsets of microbial populations including the Acidobacteria, Actinobacteria, Chloroflexi, and Gemmatimonadetes that were differentially abundant in T1C-1 and Mnghui 63 soils. Finally, the potential for T1C-1-associated root metabolites to exert growth effects on T1C-1-associated species was experimentally validated by analysis of bacterial cultures, revealing that Bt rice planting could selectively modulate specific root microbiota. Overall, this study indicate that Bt rice can directly modulate rhizosphere microbiome assemblages by altering the metabolic compositions of root exudates that then alters soil metabolite profiles and physiochemical properties. This study unveils the mechanistic associations of Bt plant-microorganism-environment, which provides comprehensive insights into the potential ecological impacts of GM plants. Nature Publishing Group UK 2023-01-23 /pmc/articles/PMC9870860/ /pubmed/36690796 http://dx.doi.org/10.1038/s43705-023-00217-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Li, Peng
Ye, Shuifeng
Chen, Jun
Wang, Luyao
Li, Yujie
Ge, Lei
Wu, Guogan
Song, Lili
Wang, Cui
Sun, Yu
Wang, Jinbin
Pan, Aihu
Quan, Zhexue
Wu, Yunfei
Combined metagenomic and metabolomic analyses reveal that Bt rice planting alters soil C-N metabolism
title Combined metagenomic and metabolomic analyses reveal that Bt rice planting alters soil C-N metabolism
title_full Combined metagenomic and metabolomic analyses reveal that Bt rice planting alters soil C-N metabolism
title_fullStr Combined metagenomic and metabolomic analyses reveal that Bt rice planting alters soil C-N metabolism
title_full_unstemmed Combined metagenomic and metabolomic analyses reveal that Bt rice planting alters soil C-N metabolism
title_short Combined metagenomic and metabolomic analyses reveal that Bt rice planting alters soil C-N metabolism
title_sort combined metagenomic and metabolomic analyses reveal that bt rice planting alters soil c-n metabolism
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9870860/
https://www.ncbi.nlm.nih.gov/pubmed/36690796
http://dx.doi.org/10.1038/s43705-023-00217-9
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