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Rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (Oreochromis niloticus) in rice-fish symbiosis

BACKGROUND: Rice-fish symbiosis, as an ecological and green aquaculture model, is an effective measure to relieve the environmental stress from intensive aquaculture. Compared with traditional aquaculture, the altered rearing pattern and environment will make differences in muscle nutrient and quali...

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Autores principales: Wang, Erlong, Zhou, Ya, Liang, Yue, Ling, Fei, Xue, Xiaoshu, He, Xianlin, Zhai, Xuliang, Xue, Yang, Zhou, Chunlong, Tang, Guo, Wang, Gaoxue
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9756501/
https://www.ncbi.nlm.nih.gov/pubmed/36527140
http://dx.doi.org/10.1186/s40168-022-01433-6
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author Wang, Erlong
Zhou, Ya
Liang, Yue
Ling, Fei
Xue, Xiaoshu
He, Xianlin
Zhai, Xuliang
Xue, Yang
Zhou, Chunlong
Tang, Guo
Wang, Gaoxue
author_facet Wang, Erlong
Zhou, Ya
Liang, Yue
Ling, Fei
Xue, Xiaoshu
He, Xianlin
Zhai, Xuliang
Xue, Yang
Zhou, Chunlong
Tang, Guo
Wang, Gaoxue
author_sort Wang, Erlong
collection PubMed
description BACKGROUND: Rice-fish symbiosis, as an ecological and green aquaculture model, is an effective measure to relieve the environmental stress from intensive aquaculture. Compared with traditional aquaculture, the altered rearing pattern and environment will make differences in muscle nutrient and quality, intestinal microbiota, body metabolism, and even disease resistance in fish. RESULTS: To investigate this, we explored the differences between rice-tilapia (aRT and bRT) and tank-tilapia (aTT and bTT) models at the periods before and after rice flowering using 16S rRNA sequencing and untargeted metabolomics. The results showed that compared with tilapia reared in the tank model, the fish body length and weight, the muscle total umami amino acid, and monounsaturated fatty acid content were obviously higher in the rice-fish model, especially after rice flowering. Compared with other groups, the intestinal microbiota diversity of fish in the bRT group was significantly higher; the dominant microbiota was Bacteroidetes and Firmicutes at the phylum level, Bacteroides and Turicibacter at the genus level, and the relative abundances of Gram-negative, potentially pathogenic, and stress-tolerant bacteria were the highest, lowest, and highest, respectively. Besides, the differential metabolite analysis indicated that rice-fish symbiosis improved the metabolic profiles and modulated the metabolic pathways in tilapia. Moreover, the correlation analysis of 16S sequencing and metabolomics showed that Bacteroides showed a positive correlation with many metabolites related to amino acid, fatty acid, and lipid metabolism. CONCLUSIONS: In summary, rice flowering improves the tilapia muscle nutrient, intestinal microbiota diversity, and disease resistance and modulates the host metabolism to acclimatize the comprehensive environment in rice-fish symbiosis. Specifically, rice flowering alters the microbiota abundance involved in amino acid, fatty acid, and lipid metabolism, resulting in improving the muscle nutrient and quality through the crosstalk of gut microbial and host metabolism. Our study will provide not only new insight into the gut microbiota-metabolism-phenotype axis, but also strong support for the promotion and application of rice-fish symbiosis in aquaculture. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01433-6.
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spelling pubmed-97565012022-12-17 Rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (Oreochromis niloticus) in rice-fish symbiosis Wang, Erlong Zhou, Ya Liang, Yue Ling, Fei Xue, Xiaoshu He, Xianlin Zhai, Xuliang Xue, Yang Zhou, Chunlong Tang, Guo Wang, Gaoxue Microbiome Research BACKGROUND: Rice-fish symbiosis, as an ecological and green aquaculture model, is an effective measure to relieve the environmental stress from intensive aquaculture. Compared with traditional aquaculture, the altered rearing pattern and environment will make differences in muscle nutrient and quality, intestinal microbiota, body metabolism, and even disease resistance in fish. RESULTS: To investigate this, we explored the differences between rice-tilapia (aRT and bRT) and tank-tilapia (aTT and bTT) models at the periods before and after rice flowering using 16S rRNA sequencing and untargeted metabolomics. The results showed that compared with tilapia reared in the tank model, the fish body length and weight, the muscle total umami amino acid, and monounsaturated fatty acid content were obviously higher in the rice-fish model, especially after rice flowering. Compared with other groups, the intestinal microbiota diversity of fish in the bRT group was significantly higher; the dominant microbiota was Bacteroidetes and Firmicutes at the phylum level, Bacteroides and Turicibacter at the genus level, and the relative abundances of Gram-negative, potentially pathogenic, and stress-tolerant bacteria were the highest, lowest, and highest, respectively. Besides, the differential metabolite analysis indicated that rice-fish symbiosis improved the metabolic profiles and modulated the metabolic pathways in tilapia. Moreover, the correlation analysis of 16S sequencing and metabolomics showed that Bacteroides showed a positive correlation with many metabolites related to amino acid, fatty acid, and lipid metabolism. CONCLUSIONS: In summary, rice flowering improves the tilapia muscle nutrient, intestinal microbiota diversity, and disease resistance and modulates the host metabolism to acclimatize the comprehensive environment in rice-fish symbiosis. Specifically, rice flowering alters the microbiota abundance involved in amino acid, fatty acid, and lipid metabolism, resulting in improving the muscle nutrient and quality through the crosstalk of gut microbial and host metabolism. Our study will provide not only new insight into the gut microbiota-metabolism-phenotype axis, but also strong support for the promotion and application of rice-fish symbiosis in aquaculture. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01433-6. BioMed Central 2022-12-16 /pmc/articles/PMC9756501/ /pubmed/36527140 http://dx.doi.org/10.1186/s40168-022-01433-6 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
Wang, Erlong
Zhou, Ya
Liang, Yue
Ling, Fei
Xue, Xiaoshu
He, Xianlin
Zhai, Xuliang
Xue, Yang
Zhou, Chunlong
Tang, Guo
Wang, Gaoxue
Rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (Oreochromis niloticus) in rice-fish symbiosis
title Rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (Oreochromis niloticus) in rice-fish symbiosis
title_full Rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (Oreochromis niloticus) in rice-fish symbiosis
title_fullStr Rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (Oreochromis niloticus) in rice-fish symbiosis
title_full_unstemmed Rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (Oreochromis niloticus) in rice-fish symbiosis
title_short Rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (Oreochromis niloticus) in rice-fish symbiosis
title_sort rice flowering improves the muscle nutrient, intestinal microbiota diversity, and liver metabolism profiles of tilapia (oreochromis niloticus) in rice-fish symbiosis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9756501/
https://www.ncbi.nlm.nih.gov/pubmed/36527140
http://dx.doi.org/10.1186/s40168-022-01433-6
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