A multi-omics spatial framework for host-microbiome dissection within the intestinal tissue microenvironment
Abstract The intricate interactions between the host immune system and its microbiome constituents undergo dynamic shifts in response to perturbations to the intestinal tissue environment. Our ability to study these events on the systems level is significantly limited by in situ approaches capable o...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2025-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-56237-7 |
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| author | Bokai Zhu Yunhao Bai Yao Yu Yeo Xiaowei Lu Xavier Rovira-Clavé Han Chen Jason Yeung Dingani Nkosi Jonathan Glickman Antonio Delgado-Gonzalez Georg K. Gerber Mike Angelo Alex K. Shalek Garry P. Nolan Sizun Jiang |
| author_facet | Bokai Zhu Yunhao Bai Yao Yu Yeo Xiaowei Lu Xavier Rovira-Clavé Han Chen Jason Yeung Dingani Nkosi Jonathan Glickman Antonio Delgado-Gonzalez Georg K. Gerber Mike Angelo Alex K. Shalek Garry P. Nolan Sizun Jiang |
| author_sort | Bokai Zhu |
| collection | DOAJ |
| description | Abstract The intricate interactions between the host immune system and its microbiome constituents undergo dynamic shifts in response to perturbations to the intestinal tissue environment. Our ability to study these events on the systems level is significantly limited by in situ approaches capable of generating simultaneous insights from both host and microbial communities. Here, we introduce Microbiome Cartography (MicroCart), a framework for simultaneous in situ probing of host and microbiome across multiple spatial modalities. We demonstrate MicroCart by investigating gut host and microbiome changes in a murine colitis model, using spatial proteomics, transcriptomics, and glycomics. Our findings reveal a global but systematic transformation in tissue immune responses, encompassing tissue-level remodeling in response to host immune and epithelial cell state perturbations, bacterial population shifts, localized inflammatory responses, and metabolic process alterations during colitis. MicroCart enables a deep investigation of the intricate interplay between the host tissue and its microbiome with spatial multi-omics. |
| format | Article |
| id | doaj-art-4716421178b94a42939b1fef34748099 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-4716421178b94a42939b1fef347480992025-02-02T12:32:26ZengNature PortfolioNature Communications2041-17232025-01-0116112010.1038/s41467-025-56237-7A multi-omics spatial framework for host-microbiome dissection within the intestinal tissue microenvironmentBokai Zhu0Yunhao Bai1Yao Yu Yeo2Xiaowei Lu3Xavier Rovira-Clavé4Han Chen5Jason Yeung6Dingani Nkosi7Jonathan Glickman8Antonio Delgado-Gonzalez9Georg K. Gerber10Mike Angelo11Alex K. Shalek12Garry P. Nolan13Sizun Jiang14Ragon Institute of MGH, MIT, and HarvardBroad Institute of MIT and HarvardCenter for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical SchoolMass Spectrometry Core Facility, Stanford UniversityDepartment of Microbiology and Immunology, Stanford UniversityDepartment of Microbiology and Immunology, Stanford UniversityCenter for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Harvard Medical SchoolDepartment of Pathology, Massachusetts General BrighamDepartment of Pathology, Massachusetts General BrighamDepartment of Microbiology and Immunology, Stanford UniversityDivision of Computational Pathology, Brigham and Women’s Hospital, Harvard Medical SchoolDepartment of Pathology, Stanford UniversityRagon Institute of MGH, MIT, and HarvardDepartment of Pathology, Stanford UniversityBroad Institute of MIT and HarvardAbstract The intricate interactions between the host immune system and its microbiome constituents undergo dynamic shifts in response to perturbations to the intestinal tissue environment. Our ability to study these events on the systems level is significantly limited by in situ approaches capable of generating simultaneous insights from both host and microbial communities. Here, we introduce Microbiome Cartography (MicroCart), a framework for simultaneous in situ probing of host and microbiome across multiple spatial modalities. We demonstrate MicroCart by investigating gut host and microbiome changes in a murine colitis model, using spatial proteomics, transcriptomics, and glycomics. Our findings reveal a global but systematic transformation in tissue immune responses, encompassing tissue-level remodeling in response to host immune and epithelial cell state perturbations, bacterial population shifts, localized inflammatory responses, and metabolic process alterations during colitis. MicroCart enables a deep investigation of the intricate interplay between the host tissue and its microbiome with spatial multi-omics.https://doi.org/10.1038/s41467-025-56237-7 |
| spellingShingle | Bokai Zhu Yunhao Bai Yao Yu Yeo Xiaowei Lu Xavier Rovira-Clavé Han Chen Jason Yeung Dingani Nkosi Jonathan Glickman Antonio Delgado-Gonzalez Georg K. Gerber Mike Angelo Alex K. Shalek Garry P. Nolan Sizun Jiang A multi-omics spatial framework for host-microbiome dissection within the intestinal tissue microenvironment Nature Communications |
| title | A multi-omics spatial framework for host-microbiome dissection within the intestinal tissue microenvironment |
| title_full | A multi-omics spatial framework for host-microbiome dissection within the intestinal tissue microenvironment |
| title_fullStr | A multi-omics spatial framework for host-microbiome dissection within the intestinal tissue microenvironment |
| title_full_unstemmed | A multi-omics spatial framework for host-microbiome dissection within the intestinal tissue microenvironment |
| title_short | A multi-omics spatial framework for host-microbiome dissection within the intestinal tissue microenvironment |
| title_sort | multi omics spatial framework for host microbiome dissection within the intestinal tissue microenvironment |
| url | https://doi.org/10.1038/s41467-025-56237-7 |
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