Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics
Abstract Functional redundancy is a key ecosystem property representing the fact that different taxa contribute to an ecosystem in similar ways through the expression of redundant functions. The redundancy of potential functions (or genome-level functional redundancy $${{{{{{\rm{FR}}}}}}}_{g}$$ FR g...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-06-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-39149-2 |
| _version_ | 1797806572515098624 |
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| author | Leyuan Li Tong Wang Zhibin Ning Xu Zhang James Butcher Joeselle M. Serrana Caitlin M. A. Simopoulos Janice Mayne Alain Stintzi David R. Mack Yang-Yu Liu Daniel Figeys |
| author_facet | Leyuan Li Tong Wang Zhibin Ning Xu Zhang James Butcher Joeselle M. Serrana Caitlin M. A. Simopoulos Janice Mayne Alain Stintzi David R. Mack Yang-Yu Liu Daniel Figeys |
| author_sort | Leyuan Li |
| collection | DOAJ |
| description | Abstract Functional redundancy is a key ecosystem property representing the fact that different taxa contribute to an ecosystem in similar ways through the expression of redundant functions. The redundancy of potential functions (or genome-level functional redundancy $${{{{{{\rm{FR}}}}}}}_{g}$$ FR g ) of human microbiomes has been recently quantified using metagenomics data. Yet, the redundancy of expressed functions in the human microbiome has never been quantitatively explored. Here, we present an approach to quantify the proteome-level functional redundancy $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p in the human gut microbiome using metaproteomics. Ultra-deep metaproteomics reveals high proteome-level functional redundancy and high nestedness in the human gut proteomic content networks (i.e., the bipartite graphs connecting taxa to functions). We find that the nested topology of proteomic content networks and relatively small functional distances between proteomes of certain pairs of taxa together contribute to high $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p in the human gut microbiome. As a metric comprehensively incorporating the factors of presence/absence of each function, protein abundances of each function and biomass of each taxon, $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p outcompetes diversity indices in detecting significant microbiome responses to environmental factors, including individuality, biogeography, xenobiotics, and disease. We show that gut inflammation and exposure to specific xenobiotics can significantly diminish the $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p with no significant change in taxonomic diversity. |
| first_indexed | 2024-03-13T06:09:18Z |
| format | Article |
| id | doaj.art-5d3f124ec93b4a05b0683ec979cc01bb |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-13T06:09:18Z |
| publishDate | 2023-06-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-5d3f124ec93b4a05b0683ec979cc01bb2023-06-11T11:19:44ZengNature PortfolioNature Communications2041-17232023-06-0114111410.1038/s41467-023-39149-2Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomicsLeyuan Li0Tong Wang1Zhibin Ning2Xu Zhang3James Butcher4Joeselle M. Serrana5Caitlin M. A. Simopoulos6Janice Mayne7Alain Stintzi8David R. Mack9Yang-Yu Liu10Daniel Figeys11State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences (Beijing), Beijing Institute of LifeomicsChanning Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical SchoolSchool of Pharmaceutical Sciences and Ottawa Institute of Systems Biology, Faculty of Medicine, University of OttawaSchool of Pharmaceutical Sciences and Ottawa Institute of Systems Biology, Faculty of Medicine, University of OttawaDepartment of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of OttawaSchool of Pharmaceutical Sciences and Ottawa Institute of Systems Biology, Faculty of Medicine, University of OttawaSchool of Pharmaceutical Sciences and Ottawa Institute of Systems Biology, Faculty of Medicine, University of OttawaSchool of Pharmaceutical Sciences and Ottawa Institute of Systems Biology, Faculty of Medicine, University of OttawaDepartment of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of OttawaDepartment of Paediatrics, Faculty of Medicine, University of Ottawa and Children’s Hospital of Eastern Ontario Inflammatory Bowel Disease Centre and Research InstituteChanning Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical SchoolSchool of Pharmaceutical Sciences and Ottawa Institute of Systems Biology, Faculty of Medicine, University of OttawaAbstract Functional redundancy is a key ecosystem property representing the fact that different taxa contribute to an ecosystem in similar ways through the expression of redundant functions. The redundancy of potential functions (or genome-level functional redundancy $${{{{{{\rm{FR}}}}}}}_{g}$$ FR g ) of human microbiomes has been recently quantified using metagenomics data. Yet, the redundancy of expressed functions in the human microbiome has never been quantitatively explored. Here, we present an approach to quantify the proteome-level functional redundancy $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p in the human gut microbiome using metaproteomics. Ultra-deep metaproteomics reveals high proteome-level functional redundancy and high nestedness in the human gut proteomic content networks (i.e., the bipartite graphs connecting taxa to functions). We find that the nested topology of proteomic content networks and relatively small functional distances between proteomes of certain pairs of taxa together contribute to high $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p in the human gut microbiome. As a metric comprehensively incorporating the factors of presence/absence of each function, protein abundances of each function and biomass of each taxon, $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p outcompetes diversity indices in detecting significant microbiome responses to environmental factors, including individuality, biogeography, xenobiotics, and disease. We show that gut inflammation and exposure to specific xenobiotics can significantly diminish the $${{{{{{\rm{FR}}}}}}}_{p}$$ FR p with no significant change in taxonomic diversity.https://doi.org/10.1038/s41467-023-39149-2 |
| spellingShingle | Leyuan Li Tong Wang Zhibin Ning Xu Zhang James Butcher Joeselle M. Serrana Caitlin M. A. Simopoulos Janice Mayne Alain Stintzi David R. Mack Yang-Yu Liu Daniel Figeys Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics Nature Communications |
| title | Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics |
| title_full | Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics |
| title_fullStr | Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics |
| title_full_unstemmed | Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics |
| title_short | Revealing proteome-level functional redundancy in the human gut microbiome using ultra-deep metaproteomics |
| title_sort | revealing proteome level functional redundancy in the human gut microbiome using ultra deep metaproteomics |
| url | https://doi.org/10.1038/s41467-023-39149-2 |
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