Deciphering the gut microbiome of grass carp through multi-omics approach
Abstract Background Aquaculture plays an important role in global protein supplies and food security. The ban on antibiotics as feed additive proposes urgent need to develop alternatives. Gut microbiota plays important roles in the metabolism and immunity of fish and has the potential to give rise t...
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-023-01715-7 |
| _version_ | 1797363120430120960 |
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| author | Ming Li Hui Liang Hongwei Yang Qianwen Ding Rui Xia Jie Chen Wenhao Zhou Yalin Yang Zhen Zhang Yuanyuan Yao Chao Ran Zhigang Zhou |
| author_facet | Ming Li Hui Liang Hongwei Yang Qianwen Ding Rui Xia Jie Chen Wenhao Zhou Yalin Yang Zhen Zhang Yuanyuan Yao Chao Ran Zhigang Zhou |
| author_sort | Ming Li |
| collection | DOAJ |
| description | Abstract Background Aquaculture plays an important role in global protein supplies and food security. The ban on antibiotics as feed additive proposes urgent need to develop alternatives. Gut microbiota plays important roles in the metabolism and immunity of fish and has the potential to give rise to novel solutions for challenges confronted by fish culture. However, our understanding of fish gut microbiome is still lacking. Results We identified 575,856 non-redundant genes by metagenomic sequencing of the intestinal content samples of grass carp. Taxonomic and functional annotation of the gene catalogue revealed specificity of the gut microbiome of grass carp compared with mammals. Co-occurrence analysis indicated exclusive relations between the genera belonging to Proteobacteria and Fusobacteria/Firmicutes/Bacteroidetes, suggesting two independent ecological groups of the microbiota. The association pattern of Proteobacteria with the gene expression modules of fish gut and the liver was consistently opposite to that of Fusobacteria, Firmicutes, and Bacteroidetes, implying differential functionality of Proteobacteria and Fusobacteria/Firmicutes/Bacteroidetes. Therefore, the two ecological groups were considered as two functional groups, i.e., Functional Group 1: Proteobacteria and Functional Group 2: Fusobacteria/Firmicutes/Bacteroidetes. Further analysis revealed that the two functional groups differ in genetic capacity for carbohydrate utilization, virulence factors, and antibiotic resistance. Finally, we proposed that the ratio of “Functional Group 2/Functional Group 1” can be used as a biomarker that efficiently reflects the structural and functional characteristics of the microbiota of grass carp. Conclusions The gene catalogue is an important resource for investigating the gut microbiome of grass carp. Multi-omics analysis provides insights into functional implications of the main phyla that comprise the fish microbiota and shed lights on targets for microbiota regulation. Video Abstract |
| first_indexed | 2024-03-08T16:16:44Z |
| format | Article |
| id | doaj.art-cd98b68ee19040b4b66caa96a3748e72 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-08T16:16:44Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-cd98b68ee19040b4b66caa96a3748e722024-01-07T12:36:03ZengBMCMicrobiome2049-26182024-01-0112111710.1186/s40168-023-01715-7Deciphering the gut microbiome of grass carp through multi-omics approachMing Li0Hui Liang1Hongwei Yang2Qianwen Ding3Rui Xia4Jie Chen5Wenhao Zhou6Yalin Yang7Zhen Zhang8Yuanyuan Yao9Chao Ran10Zhigang Zhou11China-Norway Joint Lab On Fish Gastrointestinal Microbiota, Institute of Feed Research, Chinese Academy of Agricultural SciencesChina-Norway Joint Lab On Fish Gastrointestinal Microbiota, Institute of Feed Research, Chinese Academy of Agricultural SciencesChina-Norway Joint Lab On Fish Gastrointestinal Microbiota, Institute of Feed Research, Chinese Academy of Agricultural SciencesBiotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural SciencesChina-Norway Joint Lab On Fish Gastrointestinal Microbiota, Institute of Feed Research, Chinese Academy of Agricultural SciencesChina-Norway Joint Lab On Fish Gastrointestinal Microbiota, Institute of Feed Research, Chinese Academy of Agricultural SciencesChina-Norway Joint Lab On Fish Gastrointestinal Microbiota, Institute of Feed Research, Chinese Academy of Agricultural SciencesBiotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural SciencesBiotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural SciencesBiotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural SciencesBiotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural SciencesChina-Norway Joint Lab On Fish Gastrointestinal Microbiota, Institute of Feed Research, Chinese Academy of Agricultural SciencesAbstract Background Aquaculture plays an important role in global protein supplies and food security. The ban on antibiotics as feed additive proposes urgent need to develop alternatives. Gut microbiota plays important roles in the metabolism and immunity of fish and has the potential to give rise to novel solutions for challenges confronted by fish culture. However, our understanding of fish gut microbiome is still lacking. Results We identified 575,856 non-redundant genes by metagenomic sequencing of the intestinal content samples of grass carp. Taxonomic and functional annotation of the gene catalogue revealed specificity of the gut microbiome of grass carp compared with mammals. Co-occurrence analysis indicated exclusive relations between the genera belonging to Proteobacteria and Fusobacteria/Firmicutes/Bacteroidetes, suggesting two independent ecological groups of the microbiota. The association pattern of Proteobacteria with the gene expression modules of fish gut and the liver was consistently opposite to that of Fusobacteria, Firmicutes, and Bacteroidetes, implying differential functionality of Proteobacteria and Fusobacteria/Firmicutes/Bacteroidetes. Therefore, the two ecological groups were considered as two functional groups, i.e., Functional Group 1: Proteobacteria and Functional Group 2: Fusobacteria/Firmicutes/Bacteroidetes. Further analysis revealed that the two functional groups differ in genetic capacity for carbohydrate utilization, virulence factors, and antibiotic resistance. Finally, we proposed that the ratio of “Functional Group 2/Functional Group 1” can be used as a biomarker that efficiently reflects the structural and functional characteristics of the microbiota of grass carp. Conclusions The gene catalogue is an important resource for investigating the gut microbiome of grass carp. Multi-omics analysis provides insights into functional implications of the main phyla that comprise the fish microbiota and shed lights on targets for microbiota regulation. Video Abstracthttps://doi.org/10.1186/s40168-023-01715-7Gut microbiotaGene modulesGene catalogueGrass crap |
| spellingShingle | Ming Li Hui Liang Hongwei Yang Qianwen Ding Rui Xia Jie Chen Wenhao Zhou Yalin Yang Zhen Zhang Yuanyuan Yao Chao Ran Zhigang Zhou Deciphering the gut microbiome of grass carp through multi-omics approach Microbiome Gut microbiota Gene modules Gene catalogue Grass crap |
| title | Deciphering the gut microbiome of grass carp through multi-omics approach |
| title_full | Deciphering the gut microbiome of grass carp through multi-omics approach |
| title_fullStr | Deciphering the gut microbiome of grass carp through multi-omics approach |
| title_full_unstemmed | Deciphering the gut microbiome of grass carp through multi-omics approach |
| title_short | Deciphering the gut microbiome of grass carp through multi-omics approach |
| title_sort | deciphering the gut microbiome of grass carp through multi omics approach |
| topic | Gut microbiota Gene modules Gene catalogue Grass crap |
| url | https://doi.org/10.1186/s40168-023-01715-7 |
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