Polyp and tumor microenvironment reprogramming in colorectal cancer: insights from mucosal bacteriome and metabolite crosstalk
Abstract Background Highly frequent colorectal cancer (CRC) is predicted to have 3.2 million novel cases by 2040. Tumor microenvironment (TME) bacteriome and metabolites are proposed to be involved in CRC development. In this regard, we aimed to investigate the bacteriome and metabolites of healthy,...
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| Format: | Article |
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BMC
2025-01-01
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| Series: | Annals of Clinical Microbiology and Antimicrobials |
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| Online Access: | https://doi.org/10.1186/s12941-025-00777-9 |
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| author | Hadi Feizi Hossein Samadi Kafil Andrey Plotnikov Vladimir Kataev Alexander Balkin Ekaterina Filonchikova Mohammad Ahangarzadeh Rezaee Reza Ghotaslou Mohammad Sadrkabir Hiva Kadkhoda Fadhil S. Kamounah Sergei Nikitin |
| author_facet | Hadi Feizi Hossein Samadi Kafil Andrey Plotnikov Vladimir Kataev Alexander Balkin Ekaterina Filonchikova Mohammad Ahangarzadeh Rezaee Reza Ghotaslou Mohammad Sadrkabir Hiva Kadkhoda Fadhil S. Kamounah Sergei Nikitin |
| author_sort | Hadi Feizi |
| collection | DOAJ |
| description | Abstract Background Highly frequent colorectal cancer (CRC) is predicted to have 3.2 million novel cases by 2040. Tumor microenvironment (TME) bacteriome and metabolites are proposed to be involved in CRC development. In this regard, we aimed to investigate the bacteriome and metabolites of healthy, adenomatous polyp, and CRC tissues. Methods Sixty samples including healthy (H), adenomatous polyps (AP), adenomatous polyps-adjacent (APA), cancer tumor (CT), and cancer tumor-adjacent (CA) tissues were collected and analyzed by 16 S rRNA sequencing and 1H NMR spectroscopy. Results Our results revealed that the bacteriome and metabolites of the H, AP, and CT groups were significantly different. We observed that the Lachnospiraceae family depleted concomitant with acetoacetate and beta-hydroxybutyric acid (BHB) accumulations in the AP tissues. In addition, some bacterial species including Gemella morbillorum, and Morganella morganii were enriched in the AP compared to the H group. Furthermore, fumarate was accumulated concomitant to Aeromonas enteropelogenes, Aeromonas veronii, and Fusobacterium nucleatum subsp. animalis increased abundance in the CT compared to the H group. Conclusion These results proposed that beneficial bacteria including the Lachnospiraceae family depletion cross-talk with acetoacetate and BHB accumulations followed by an increased abundance of driver bacteria including G. morbillorum, and M. morganii may reprogram polyp microenvironment leading to tumor initiation. Consequently, passenger bacteria accumulation like A. enteropelogenes, A.veronii, and F. nucleatum subsp. animalis cross-talking fumarate in the TME may aggravate cancer development. So, knowledge of TME bacteriome and metabolites might help in cancer prevention, early diagnosis, and a good prognosis. |
| format | Article |
| id | doaj-art-3fadafbbcedf469487b4989df77c60c2 |
| institution | Kabale University |
| issn | 1476-0711 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Annals of Clinical Microbiology and Antimicrobials |
| spelling | doaj-art-3fadafbbcedf469487b4989df77c60c22025-02-02T12:12:28ZengBMCAnnals of Clinical Microbiology and Antimicrobials1476-07112025-01-0124111710.1186/s12941-025-00777-9Polyp and tumor microenvironment reprogramming in colorectal cancer: insights from mucosal bacteriome and metabolite crosstalkHadi Feizi0Hossein Samadi Kafil1Andrey Plotnikov2Vladimir Kataev3Alexander Balkin4Ekaterina Filonchikova5Mohammad Ahangarzadeh Rezaee6Reza Ghotaslou7Mohammad Sadrkabir8Hiva Kadkhoda9Fadhil S. Kamounah10Sergei Nikitin11Drug Applied Research Center, Faculty of Medicine, Tabriz University of Medical SciencesDrug Applied Research Center, Faculty of Medicine, Tabriz University of Medical SciencesInstitute for Cellular and Intracellular Symbiosis of the Ural Branch of the Russian Academy of SciencesInstitute for Cellular and Intracellular Symbiosis of the Ural Branch of the Russian Academy of SciencesInstitute for Cellular and Intracellular Symbiosis of the Ural Branch of the Russian Academy of SciencesInstitute for Cellular and Intracellular Symbiosis of the Ural Branch of the Russian Academy of SciencesDepartment of Bacteriology and Virology, Faculty of Medicine, Tabriz University of Medical SciencesDepartment of Bacteriology and Virology, Faculty of Medicine, Tabriz University of Medical SciencesDepartment of Internal Medicine, Tabriz Branch, Islamic Azad UniversityDrug Applied Research Center, Faculty of Medicine, Tabriz University of Medical SciencesDepartment of Chemistry, University of CopenhagenDepartment of Science and Environment, Roskilde UniversityAbstract Background Highly frequent colorectal cancer (CRC) is predicted to have 3.2 million novel cases by 2040. Tumor microenvironment (TME) bacteriome and metabolites are proposed to be involved in CRC development. In this regard, we aimed to investigate the bacteriome and metabolites of healthy, adenomatous polyp, and CRC tissues. Methods Sixty samples including healthy (H), adenomatous polyps (AP), adenomatous polyps-adjacent (APA), cancer tumor (CT), and cancer tumor-adjacent (CA) tissues were collected and analyzed by 16 S rRNA sequencing and 1H NMR spectroscopy. Results Our results revealed that the bacteriome and metabolites of the H, AP, and CT groups were significantly different. We observed that the Lachnospiraceae family depleted concomitant with acetoacetate and beta-hydroxybutyric acid (BHB) accumulations in the AP tissues. In addition, some bacterial species including Gemella morbillorum, and Morganella morganii were enriched in the AP compared to the H group. Furthermore, fumarate was accumulated concomitant to Aeromonas enteropelogenes, Aeromonas veronii, and Fusobacterium nucleatum subsp. animalis increased abundance in the CT compared to the H group. Conclusion These results proposed that beneficial bacteria including the Lachnospiraceae family depletion cross-talk with acetoacetate and BHB accumulations followed by an increased abundance of driver bacteria including G. morbillorum, and M. morganii may reprogram polyp microenvironment leading to tumor initiation. Consequently, passenger bacteria accumulation like A. enteropelogenes, A.veronii, and F. nucleatum subsp. animalis cross-talking fumarate in the TME may aggravate cancer development. So, knowledge of TME bacteriome and metabolites might help in cancer prevention, early diagnosis, and a good prognosis.https://doi.org/10.1186/s12941-025-00777-9Colorectal cancerGut microbiomeGut metabolomeTumor microenvironmentFusobacterium nucleatum |
| spellingShingle | Hadi Feizi Hossein Samadi Kafil Andrey Plotnikov Vladimir Kataev Alexander Balkin Ekaterina Filonchikova Mohammad Ahangarzadeh Rezaee Reza Ghotaslou Mohammad Sadrkabir Hiva Kadkhoda Fadhil S. Kamounah Sergei Nikitin Polyp and tumor microenvironment reprogramming in colorectal cancer: insights from mucosal bacteriome and metabolite crosstalk Annals of Clinical Microbiology and Antimicrobials Colorectal cancer Gut microbiome Gut metabolome Tumor microenvironment Fusobacterium nucleatum |
| title | Polyp and tumor microenvironment reprogramming in colorectal cancer: insights from mucosal bacteriome and metabolite crosstalk |
| title_full | Polyp and tumor microenvironment reprogramming in colorectal cancer: insights from mucosal bacteriome and metabolite crosstalk |
| title_fullStr | Polyp and tumor microenvironment reprogramming in colorectal cancer: insights from mucosal bacteriome and metabolite crosstalk |
| title_full_unstemmed | Polyp and tumor microenvironment reprogramming in colorectal cancer: insights from mucosal bacteriome and metabolite crosstalk |
| title_short | Polyp and tumor microenvironment reprogramming in colorectal cancer: insights from mucosal bacteriome and metabolite crosstalk |
| title_sort | polyp and tumor microenvironment reprogramming in colorectal cancer insights from mucosal bacteriome and metabolite crosstalk |
| topic | Colorectal cancer Gut microbiome Gut metabolome Tumor microenvironment Fusobacterium nucleatum |
| url | https://doi.org/10.1186/s12941-025-00777-9 |
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