Parvimonas micra can translocate from the subgingival sulcus of the human oral cavity to colorectal adenocarcinoma

Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non‐CRC) were collected for microbiome analysis. Saliva (28 non‐CRC and 94 CRC), feces (30 non‐CRC and 97 CRC), subgingival fluid (20 CRC), and tumor tissue samples (20 CRC) were used for 16S me...

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Published inMolecular oncology Vol. 18; no. 5; pp. 1143 - 1173
Main Authors Conde‐Pérez, Kelly, Buetas, Elena, Aja‐Macaya, Pablo, Martin‐De Arribas, Elsa, Iglesias‐Corrás, Iago, Trigo‐Tasende, Noelia, Nasser‐Ali, Mohammed, Estévez, Lara S., Rumbo‐Feal, Soraya, Otero‐Alén, Begoña, Noguera, Jose F., Concha, Ángel, Pardiñas‐López, Simón, Carda‐Diéguez, Miguel, Gómez‐Randulfe, Igor, Martínez‐Lago, Nieves, Ladra, Susana, Aparicio, Luis A., Bou, Germán, Mira, Alex, Vallejo, Juan A., Poza, Margarita
Format Journal Article
LanguageEnglish
Published United States John Wiley & Sons, Inc 01.05.2024
John Wiley and Sons Inc
Wiley
Subjects
Online AccessGet full text
ISSN1574-7891
1878-0261
1878-0261
DOI10.1002/1878-0261.13506

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Abstract Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non‐CRC) were collected for microbiome analysis. Saliva (28 non‐CRC and 94 CRC), feces (30 non‐CRC and 97 CRC), subgingival fluid (20 CRC), and tumor tissue samples (20 CRC) were used for 16S metabarcoding and/or RNA sequencing (RNAseq) approaches. A differential analysis of the abundance, performed with the ANCOM‐BC package, adjusting the P‐values by the Holm‐Bonferroni method, revealed that Parvimonas was significantly over‐represented in feces from CRC patients (P‐value < 0.001) compared to healthy controls. A total of 11 Parvimonas micra isolates were obtained from the oral cavity and adenocarcinoma of CRC patients. Genome analysis identified a pair of isolates from the same patient that shared 99.2% identity, demonstrating that P. micra can translocate from the subgingival cavity to the gut. The data suggest that P. micra could migrate in a synergistic consortium with other periodontal bacteria. Metatranscriptomics confirmed that oral bacteria were more active in tumor than in non‐neoplastic tissues. We suggest that P. micra could be considered as a CRC biomarker detected in non‐invasive samples such as feces. Parvimonas micra can translocate from the oral cavity to the intestinal lumen, through the circulatory or gastrointestinal system, where the anaerobic bacteria undergoes some genome and transcriptomic changes needed for the adaptation to its new niche. P. micra can be considered as an excellent CRC biomarker detected in non‐invasive samples.
AbstractList Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non‐CRC) were collected for microbiome analysis. Saliva (28 non‐CRC and 94 CRC), feces (30 non‐CRC and 97 CRC), subgingival fluid (20 CRC), and tumor tissue samples (20 CRC) were used for 16S metabarcoding and/or RNA sequencing (RNAseq) approaches. A differential analysis of the abundance, performed with the ANCOM‐BC package, adjusting the P ‐values by the Holm‐Bonferroni method, revealed that Parvimonas was significantly over‐represented in feces from CRC patients ( P ‐value < 0.001) compared to healthy controls. A total of 11 Parvimonas micra isolates were obtained from the oral cavity and adenocarcinoma of CRC patients. Genome analysis identified a pair of isolates from the same patient that shared 99.2% identity, demonstrating that P. micra can translocate from the subgingival cavity to the gut. The data suggest that P. micra could migrate in a synergistic consortium with other periodontal bacteria. Metatranscriptomics confirmed that oral bacteria were more active in tumor than in non‐neoplastic tissues. We suggest that P. micra could be considered as a CRC biomarker detected in non‐invasive samples such as feces.
Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non-CRC) were collected for microbiome analysis. Saliva (28 non-CRC and 94 CRC), feces (30 non-CRC and 97 CRC), subgingival fluid (20 CRC), and tumor tissue samples (20 CRC) were used for 16S metabarcoding and/or RNA sequencing (RNAseq) approaches. A differential analysis of the abundance, performed with the ANCOM-BC package, adjusting the P-values by the Holm-Bonferroni method, revealed that Parvimonas was significantly over-represented in feces from CRC patients (P-value < 0.001) compared to healthy controls. A total of 11 Parvimonas micra isolates were obtained from the oral cavity and adenocarcinoma of CRC patients. Genome analysis identified a pair of isolates from the same patient that shared 99.2% identity, demonstrating that P. micra can translocate from the subgingival cavity to the gut. The data suggest that P. micra could migrate in a synergistic consortium with other periodontal bacteria. Metatranscriptomics confirmed that oral bacteria were more active in tumor than in non-neoplastic tissues. We suggest that P. micra could be considered as a CRC biomarker detected in non-invasive samples such as feces.Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non-CRC) were collected for microbiome analysis. Saliva (28 non-CRC and 94 CRC), feces (30 non-CRC and 97 CRC), subgingival fluid (20 CRC), and tumor tissue samples (20 CRC) were used for 16S metabarcoding and/or RNA sequencing (RNAseq) approaches. A differential analysis of the abundance, performed with the ANCOM-BC package, adjusting the P-values by the Holm-Bonferroni method, revealed that Parvimonas was significantly over-represented in feces from CRC patients (P-value < 0.001) compared to healthy controls. A total of 11 Parvimonas micra isolates were obtained from the oral cavity and adenocarcinoma of CRC patients. Genome analysis identified a pair of isolates from the same patient that shared 99.2% identity, demonstrating that P. micra can translocate from the subgingival cavity to the gut. The data suggest that P. micra could migrate in a synergistic consortium with other periodontal bacteria. Metatranscriptomics confirmed that oral bacteria were more active in tumor than in non-neoplastic tissues. We suggest that P. micra could be considered as a CRC biomarker detected in non-invasive samples such as feces.
Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non‐CRC) were collected for microbiome analysis. Saliva (28 non‐CRC and 94 CRC), feces (30 non‐CRC and 97 CRC), subgingival fluid (20 CRC), and tumor tissue samples (20 CRC) were used for 16S metabarcoding and/or RNA sequencing (RNAseq) approaches. A differential analysis of the abundance, performed with the ANCOM‐BC package, adjusting the P ‐values by the Holm‐Bonferroni method, revealed that Parvimonas was significantly over‐represented in feces from CRC patients ( P ‐value < 0.001) compared to healthy controls. A total of 11 Parvimonas micra isolates were obtained from the oral cavity and adenocarcinoma of CRC patients. Genome analysis identified a pair of isolates from the same patient that shared 99.2% identity, demonstrating that P. micra can translocate from the subgingival cavity to the gut. The data suggest that P. micra could migrate in a synergistic consortium with other periodontal bacteria. Metatranscriptomics confirmed that oral bacteria were more active in tumor than in non‐neoplastic tissues. We suggest that P. micra could be considered as a CRC biomarker detected in non‐invasive samples such as feces. Parvimonas micra can translocate from the oral cavity to the intestinal lumen, through the circulatory or gastrointestinal system, where the anaerobic bacteria undergoes some genome and transcriptomic changes needed for the adaptation to its new niche. P. micra can be considered as an excellent CRC biomarker detected in non‐invasive samples.
Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non‐CRC) were collected for microbiome analysis. Saliva (28 non‐CRC and 94 CRC), feces (30 non‐CRC and 97 CRC), subgingival fluid (20 CRC), and tumor tissue samples (20 CRC) were used for 16S metabarcoding and/or RNA sequencing (RNAseq) approaches. A differential analysis of the abundance, performed with the ANCOM‐BC package, adjusting the P‐values by the Holm‐Bonferroni method, revealed that Parvimonas was significantly over‐represented in feces from CRC patients (P‐value < 0.001) compared to healthy controls. A total of 11 Parvimonas micra isolates were obtained from the oral cavity and adenocarcinoma of CRC patients. Genome analysis identified a pair of isolates from the same patient that shared 99.2% identity, demonstrating that P. micra can translocate from the subgingival cavity to the gut. The data suggest that P. micra could migrate in a synergistic consortium with other periodontal bacteria. Metatranscriptomics confirmed that oral bacteria were more active in tumor than in non‐neoplastic tissues. We suggest that P. micra could be considered as a CRC biomarker detected in non‐invasive samples such as feces.
Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non‐CRC) were collected for microbiome analysis. Saliva (28 non‐CRC and 94 CRC), feces (30 non‐CRC and 97 CRC), subgingival fluid (20 CRC), and tumor tissue samples (20 CRC) were used for 16S metabarcoding and/or RNA sequencing (RNAseq) approaches. A differential analysis of the abundance, performed with the ANCOM‐BC package, adjusting the P‐values by the Holm‐Bonferroni method, revealed that Parvimonas was significantly over‐represented in feces from CRC patients (P‐value < 0.001) compared to healthy controls. A total of 11 Parvimonas micra isolates were obtained from the oral cavity and adenocarcinoma of CRC patients. Genome analysis identified a pair of isolates from the same patient that shared 99.2% identity, demonstrating that P. micra can translocate from the subgingival cavity to the gut. The data suggest that P. micra could migrate in a synergistic consortium with other periodontal bacteria. Metatranscriptomics confirmed that oral bacteria were more active in tumor than in non‐neoplastic tissues. We suggest that P. micra could be considered as a CRC biomarker detected in non‐invasive samples such as feces. Parvimonas micra can translocate from the oral cavity to the intestinal lumen, through the circulatory or gastrointestinal system, where the anaerobic bacteria undergoes some genome and transcriptomic changes needed for the adaptation to its new niche. P. micra can be considered as an excellent CRC biomarker detected in non‐invasive samples.
Audience Academic
Author Trigo‐Tasende, Noelia
Vallejo, Juan A.
Estévez, Lara S.
Pardiñas‐López, Simón
Martínez‐Lago, Nieves
Ladra, Susana
Martin‐De Arribas, Elsa
Otero‐Alén, Begoña
Aja‐Macaya, Pablo
Conde‐Pérez, Kelly
Noguera, Jose F.
Concha, Ángel
Carda‐Diéguez, Miguel
Buetas, Elena
Aparicio, Luis A.
Poza, Margarita
Nasser‐Ali, Mohammed
Iglesias‐Corrás, Iago
Rumbo‐Feal, Soraya
Gómez‐Randulfe, Igor
Bou, Germán
Mira, Alex
AuthorAffiliation 4 Pathological Anatomy Service and Biobank University Hospital of A Coruña (HUAC), Institute of Biomedical Research (INIBIC), Hospital Universitario Spain
7 Medical Oncology Department University Hospital of A Coruña (HUAC), Maternal and Child Hospital Spain
3 Database Laboratory Research Center for Information and Communication Technologies (CITIC), University of A Coruña (UDC), Campus de Elviña Spain
5 General and Digestive Surgery Service University Hospital of A Coruña (HUAC), Hospital Universitario Spain
1 meiGAbiome, Microbiology Research Group, Servicio de Microbiología Center for Advanced Scientific Research (CICA), Institute of Biomedical Research (INIBIC), University Hospital of A Coruña (HUAC), University of A Coruña (UDC), CIBER of Infectious Diseases (CIBERINFEC‐ISCIII), Hospital Universitario Spain
6 Periodontology and Oral Surgery Pardiñas Medical Dental Clinic, Cell Therapy and Regenerative Medicine Group, Institute of Biomedical Research (INIBIC) A Coruña Spain
8 Microbiome
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37558206$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2023 The Authors. published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
2023 The Authors. Molecular Oncology published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
COPYRIGHT 2024 John Wiley & Sons, Inc.
2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: 2023 The Authors. published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
– notice: 2023 The Authors. Molecular Oncology published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
– notice: COPYRIGHT 2024 John Wiley & Sons, Inc.
– notice: 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Issue 5
Keywords Parvimonas micra
metabarcoding
colorectal cancer
metatranscriptomics
microbiome
periodontal disease
Language English
License Attribution
2023 The Authors. Molecular Oncology published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Notes Kelly Conde‐Pérez, Elena Buetas and Pablo Aja‐Macaya contributed equally as first authors of this work
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Snippet Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non‐CRC) were collected for microbiome analysis....
Oral and intestinal samples from a cohort of 93 colorectal cancer (CRC) patients and 30 healthy controls (non-CRC) were collected for microbiome analysis....
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SubjectTerms Adenocarcinoma
Adenocarcinoma - microbiology
Adenocarcinoma - pathology
Aged
Antibiotics
Bacteria
Biomarkers
Cancer therapies
Colorectal cancer
Colorectal carcinoma
Colorectal Neoplasms - microbiology
Colorectal Neoplasms - pathology
Comparative analysis
CRISPR
Development and progression
DNA methylation
Feces
Feces - microbiology
Female
Firmicutes
Genomes
Genomics
Gingiva
Gingiva - microbiology
Gingiva - pathology
Gum disease
Hospitals
Humans
Immune system
Immunology
Inflammation
Male
Medical prognosis
metabarcoding
Metastasis
metatranscriptomics
microbiome
Microbiomes
Microbiota
Middle Aged
Mouth - microbiology
Oral cavity
Parvimonas micra
Pathogens
Peptostreptococcus - genetics
Peptostreptococcus - isolation & purification
periodontal disease
Phreatodrobia micra
RNA
RNA sequencing
RNA, Ribosomal, 16S - genetics
Saliva
Saliva - microbiology
Scientific equipment and supplies industry
Tumors
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Title Parvimonas micra can translocate from the subgingival sulcus of the human oral cavity to colorectal adenocarcinoma
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2F1878-0261.13506
https://www.ncbi.nlm.nih.gov/pubmed/37558206
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Volume 18
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