Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets
Abstract Background Colorectal cancer (CRC) risk is strongly affected by dietary habits with red and processed meat increasing risk, and foods rich in dietary fibres considered protective. Dietary habits also shape gut microbiota, but the role of the combination between diet, the gut microbiota, and...
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2024-09-01
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| Series: | Microbiome |
| Online Access: | https://doi.org/10.1186/s40168-024-01900-2 |
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| author | Carlotta De Filippo Sofia Chioccioli Niccolò Meriggi Antonio Dario Troise Francesco Vitali Mariela Mejia Monroy Serdar Özsezen Katia Tortora Aurélie Balvay Claire Maudet Nathalie Naud Edwin Fouché Charline Buisson Jacques Dupuy Valérie Bézirard Sylvie Chevolleau Valérie Tondereau Vassilia Theodorou Claire Maslo Perrine Aubry Camille Etienne Lisa Giovannelli Vincenzo Longo Andrea Scaloni Duccio Cavalieri Jildau Bouwman Fabrice Pierre Philippe Gérard Françoise Guéraud Giovanna Caderni |
| author_facet | Carlotta De Filippo Sofia Chioccioli Niccolò Meriggi Antonio Dario Troise Francesco Vitali Mariela Mejia Monroy Serdar Özsezen Katia Tortora Aurélie Balvay Claire Maudet Nathalie Naud Edwin Fouché Charline Buisson Jacques Dupuy Valérie Bézirard Sylvie Chevolleau Valérie Tondereau Vassilia Theodorou Claire Maslo Perrine Aubry Camille Etienne Lisa Giovannelli Vincenzo Longo Andrea Scaloni Duccio Cavalieri Jildau Bouwman Fabrice Pierre Philippe Gérard Françoise Guéraud Giovanna Caderni |
| author_sort | Carlotta De Filippo |
| collection | DOAJ |
| description | Abstract Background Colorectal cancer (CRC) risk is strongly affected by dietary habits with red and processed meat increasing risk, and foods rich in dietary fibres considered protective. Dietary habits also shape gut microbiota, but the role of the combination between diet, the gut microbiota, and the metabolite profile on CRC risk is still missing an unequivocal characterisation. Methods To investigate how gut microbiota affects diet-associated CRC risk, we fed Apc-mutated PIRC rats and azoxymethane (AOM)-induced rats the following diets: a high-risk red/processed meat-based diet (MBD), a normalised risk diet (MBD with α-tocopherol, MBDT), a low-risk pesco-vegetarian diet (PVD), and control diet. We then conducted faecal microbiota transplantation (FMT) from PIRC rats to germ-free rats treated with AOM and fed a standard diet for 3 months. We analysed multiple tumour markers and assessed the variations in the faecal microbiota using 16S rRNA gene sequencing together with targeted- and untargeted-metabolomics analyses. Results In both animal models, the PVD group exhibited significantly lower colon tumorigenesis than the MBD ones, consistent with various CRC biomarkers. Faecal microbiota and its metabolites also revealed significant diet-dependent profiles. Intriguingly, when faeces from PIRC rats fed these diets were transplanted into germ-free rats, those transplanted with MBD faeces developed a higher number of preneoplastic lesions together with distinctive diet-related bacterial and metabolic profiles. PVD determines a selection of nine taxonomic markers mainly belonging to Lachnospiraceae and Prevotellaceae families exclusively associated with at least two different animal models, and within these, four taxonomic markers were shared across all the three animal models. An inverse correlation between nonconjugated bile acids and bacterial genera mainly belonging to the Lachnospiraceae and Prevotellaceae families (representative of the PVD group) was present, suggesting a potential mechanism of action for the protective effect of these genera against CRC. Conclusions These results highlight the protective effects of PVD while reaffirming the carcinogenic properties of MBD diets. In germ-free rats, FMT induced changes reminiscent of dietary effects, including heightened preneoplastic lesions in MBD rats and the transmission of specific diet-related bacterial and metabolic profiles. Importantly, to the best of our knowledge, this is the first study showing that diet-associated cancer risk can be transferred with faeces, establishing gut microbiota as a determinant of diet-associated CRC risk. Therefore, this study marks the pioneering demonstration of faecal transfer as a means of conveying diet-related cancer risk, firmly establishing the gut microbiota as a pivotal factor in diet-associated CRC susceptibility. Video Abstract |
| format | Article |
| id | doaj-art-37d9a245919b4314b7a2937cd4b555b1 |
| institution | Kabale University |
| issn | 2049-2618 |
| language | English |
| publishDate | 2024-09-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj-art-37d9a245919b4314b7a2937cd4b555b12025-01-26T12:43:14ZengBMCMicrobiome2049-26182024-09-0112112410.1186/s40168-024-01900-2Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian dietsCarlotta De Filippo0Sofia Chioccioli1Niccolò Meriggi2Antonio Dario Troise3Francesco Vitali4Mariela Mejia Monroy5Serdar Özsezen6Katia Tortora7Aurélie Balvay8Claire Maudet9Nathalie Naud10Edwin Fouché11Charline Buisson12Jacques Dupuy13Valérie Bézirard14Sylvie Chevolleau15Valérie Tondereau16Vassilia Theodorou17Claire Maslo18Perrine Aubry19Camille Etienne20Lisa Giovannelli21Vincenzo Longo22Andrea Scaloni23Duccio Cavalieri24Jildau Bouwman25Fabrice Pierre26Philippe Gérard27Françoise Guéraud28Giovanna Caderni29Institute of Agricultural Biology and Biotechnology (IBBA), National Research Council (CNR)NEUROFARBA Department, Pharmacology and Toxicology Section, University of FlorenceInstitute of Agricultural Biology and Biotechnology (IBBA), National Research Council (CNR)Proteomics, Metabolomics and Mass Spectrometry Laboratory, ISPAAM, National Research CouncilInstitute of Agricultural Biology and Biotechnology (IBBA), National Research Council (CNR)Institute of Agricultural Biology and Biotechnology (IBBA), National Research Council (CNR)Netherlands Organisation for Applied Scientific ResearchNEUROFARBA Department, Pharmacology and Toxicology Section, University of FlorenceMicalis Institute, INRAE, AgroParisTech, Université Paris-SaclayMicalis Institute, INRAE, AgroParisTech, Université Paris-SaclayToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityMicalis Institute, INRAE, AgroParisTech, Université Paris-SaclayNEUROFARBA Department, Pharmacology and Toxicology Section, University of FlorenceInstitute of Agricultural Biology and Biotechnology (IBBA), National Research Council (CNR)Proteomics, Metabolomics and Mass Spectrometry Laboratory, ISPAAM, National Research CouncilDepartment of Biology, University of FlorenceNetherlands Organisation for Applied Scientific ResearchToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityMicalis Institute, INRAE, AgroParisTech, Université Paris-SaclayToxalim, INRAE, ENVT, INP-Purpan, UPS, Toulouse UniversityNEUROFARBA Department, Pharmacology and Toxicology Section, University of FlorenceAbstract Background Colorectal cancer (CRC) risk is strongly affected by dietary habits with red and processed meat increasing risk, and foods rich in dietary fibres considered protective. Dietary habits also shape gut microbiota, but the role of the combination between diet, the gut microbiota, and the metabolite profile on CRC risk is still missing an unequivocal characterisation. Methods To investigate how gut microbiota affects diet-associated CRC risk, we fed Apc-mutated PIRC rats and azoxymethane (AOM)-induced rats the following diets: a high-risk red/processed meat-based diet (MBD), a normalised risk diet (MBD with α-tocopherol, MBDT), a low-risk pesco-vegetarian diet (PVD), and control diet. We then conducted faecal microbiota transplantation (FMT) from PIRC rats to germ-free rats treated with AOM and fed a standard diet for 3 months. We analysed multiple tumour markers and assessed the variations in the faecal microbiota using 16S rRNA gene sequencing together with targeted- and untargeted-metabolomics analyses. Results In both animal models, the PVD group exhibited significantly lower colon tumorigenesis than the MBD ones, consistent with various CRC biomarkers. Faecal microbiota and its metabolites also revealed significant diet-dependent profiles. Intriguingly, when faeces from PIRC rats fed these diets were transplanted into germ-free rats, those transplanted with MBD faeces developed a higher number of preneoplastic lesions together with distinctive diet-related bacterial and metabolic profiles. PVD determines a selection of nine taxonomic markers mainly belonging to Lachnospiraceae and Prevotellaceae families exclusively associated with at least two different animal models, and within these, four taxonomic markers were shared across all the three animal models. An inverse correlation between nonconjugated bile acids and bacterial genera mainly belonging to the Lachnospiraceae and Prevotellaceae families (representative of the PVD group) was present, suggesting a potential mechanism of action for the protective effect of these genera against CRC. Conclusions These results highlight the protective effects of PVD while reaffirming the carcinogenic properties of MBD diets. In germ-free rats, FMT induced changes reminiscent of dietary effects, including heightened preneoplastic lesions in MBD rats and the transmission of specific diet-related bacterial and metabolic profiles. Importantly, to the best of our knowledge, this is the first study showing that diet-associated cancer risk can be transferred with faeces, establishing gut microbiota as a determinant of diet-associated CRC risk. Therefore, this study marks the pioneering demonstration of faecal transfer as a means of conveying diet-related cancer risk, firmly establishing the gut microbiota as a pivotal factor in diet-associated CRC susceptibility. Video Abstracthttps://doi.org/10.1186/s40168-024-01900-2 |
| spellingShingle | Carlotta De Filippo Sofia Chioccioli Niccolò Meriggi Antonio Dario Troise Francesco Vitali Mariela Mejia Monroy Serdar Özsezen Katia Tortora Aurélie Balvay Claire Maudet Nathalie Naud Edwin Fouché Charline Buisson Jacques Dupuy Valérie Bézirard Sylvie Chevolleau Valérie Tondereau Vassilia Theodorou Claire Maslo Perrine Aubry Camille Etienne Lisa Giovannelli Vincenzo Longo Andrea Scaloni Duccio Cavalieri Jildau Bouwman Fabrice Pierre Philippe Gérard Françoise Guéraud Giovanna Caderni Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets Microbiome |
| title | Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets |
| title_full | Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets |
| title_fullStr | Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets |
| title_full_unstemmed | Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets |
| title_short | Gut microbiota drives colon cancer risk associated with diet: a comparative analysis of meat-based and pesco-vegetarian diets |
| title_sort | gut microbiota drives colon cancer risk associated with diet a comparative analysis of meat based and pesco vegetarian diets |
| url | https://doi.org/10.1186/s40168-024-01900-2 |
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