Cargando…

Microbial dynamics with CRC progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls

Accumulating evidence has related the gut microbiota to colorectal cancer (CRC). Fusobacterium nucleatum has repeatedly been linked to colorectal tumorigenesis. The aim of this study was to investigate microbial composition in different sampling sites, in order to profile the microbial dynamics with...

Descripción completa

Detalles Bibliográficos
Autores principales: Senthakumaran, Thulasika, Moen, Aina E. F., Tannæs, Tone M., Endres, Alexander, Brackmann, Stephan A., Rounge, Trine B., Bemanian, Vahid, Tunsjø, Hege S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9899194/
https://www.ncbi.nlm.nih.gov/pubmed/36703031
http://dx.doi.org/10.1007/s10096-023-04551-7
_version_ 1784882589456138240
author Senthakumaran, Thulasika
Moen, Aina E. F.
Tannæs, Tone M.
Endres, Alexander
Brackmann, Stephan A.
Rounge, Trine B.
Bemanian, Vahid
Tunsjø, Hege S.
author_facet Senthakumaran, Thulasika
Moen, Aina E. F.
Tannæs, Tone M.
Endres, Alexander
Brackmann, Stephan A.
Rounge, Trine B.
Bemanian, Vahid
Tunsjø, Hege S.
author_sort Senthakumaran, Thulasika
collection PubMed
description Accumulating evidence has related the gut microbiota to colorectal cancer (CRC). Fusobacterium nucleatum has repeatedly been linked to colorectal tumorigenesis. The aim of this study was to investigate microbial composition in different sampling sites, in order to profile the microbial dynamics with CRC progression. Further, we characterized the tumor-associated F. nucleatum subspecies. Here, we conducted Illumina Miseq next-generation sequencing of the 16S rRNA V4 region in biopsy samples, to investigate microbiota alterations in cancer patients, patients with adenomatous polyp, and healthy controls in Norway. Further, Fusobacterium positive tumor biopsies were subjected to MinION nanopore sequencing of Fusobacterium-specific amplicons to characterize the Fusobacterium species and subspecies. We found enrichment of oral biofilm-associated bacteria, Fusobacterium, Gemella, Parvimonas, Granulicatella, Leptotrichia, Peptostreptococcus, Campylobacter, Selenomonas, Porphyromonas, and Prevotella in cancer patients compared to adenomatous polyp patients and control patients. Higher abundance of amplicon sequence variants (ASVs) classified as Phascolarctobacterium, Bacteroides vulgatus, Bacteroides plebeius, Bacteroides eggerthii, Tyzzerella, Desulfovibrio, Frisingicoccus, Eubacterium coprostanoligenes group, and Lachnospiraceae were identified in cancer and adenomatous polyp patients compared to healthy controls. F. nucleatum ssp. animalis was the dominating subspecies. F. nucleatum ssp. nucleatum, F. nucleatum ssp. vincentii, Fusobacterium pseudoperiodonticum, Fusobacterium necrophorum, and Fusobacterium gonidiaformans were identified in five samples. Several biofilm-associated bacteria were enriched at multiple sites in cancer patients. Another group of bacteria was enriched in both cancer and polyps, suggesting that they may have a role in polyp development and possibly early stages of CRC. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10096-023-04551-7.
format Online
Article
Text
id pubmed-9899194
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Springer Berlin Heidelberg
record_format MEDLINE/PubMed
spelling pubmed-98991942023-02-06 Microbial dynamics with CRC progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls Senthakumaran, Thulasika Moen, Aina E. F. Tannæs, Tone M. Endres, Alexander Brackmann, Stephan A. Rounge, Trine B. Bemanian, Vahid Tunsjø, Hege S. Eur J Clin Microbiol Infect Dis Original Article Accumulating evidence has related the gut microbiota to colorectal cancer (CRC). Fusobacterium nucleatum has repeatedly been linked to colorectal tumorigenesis. The aim of this study was to investigate microbial composition in different sampling sites, in order to profile the microbial dynamics with CRC progression. Further, we characterized the tumor-associated F. nucleatum subspecies. Here, we conducted Illumina Miseq next-generation sequencing of the 16S rRNA V4 region in biopsy samples, to investigate microbiota alterations in cancer patients, patients with adenomatous polyp, and healthy controls in Norway. Further, Fusobacterium positive tumor biopsies were subjected to MinION nanopore sequencing of Fusobacterium-specific amplicons to characterize the Fusobacterium species and subspecies. We found enrichment of oral biofilm-associated bacteria, Fusobacterium, Gemella, Parvimonas, Granulicatella, Leptotrichia, Peptostreptococcus, Campylobacter, Selenomonas, Porphyromonas, and Prevotella in cancer patients compared to adenomatous polyp patients and control patients. Higher abundance of amplicon sequence variants (ASVs) classified as Phascolarctobacterium, Bacteroides vulgatus, Bacteroides plebeius, Bacteroides eggerthii, Tyzzerella, Desulfovibrio, Frisingicoccus, Eubacterium coprostanoligenes group, and Lachnospiraceae were identified in cancer and adenomatous polyp patients compared to healthy controls. F. nucleatum ssp. animalis was the dominating subspecies. F. nucleatum ssp. nucleatum, F. nucleatum ssp. vincentii, Fusobacterium pseudoperiodonticum, Fusobacterium necrophorum, and Fusobacterium gonidiaformans were identified in five samples. Several biofilm-associated bacteria were enriched at multiple sites in cancer patients. Another group of bacteria was enriched in both cancer and polyps, suggesting that they may have a role in polyp development and possibly early stages of CRC. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10096-023-04551-7. Springer Berlin Heidelberg 2023-01-27 2023 /pmc/articles/PMC9899194/ /pubmed/36703031 http://dx.doi.org/10.1007/s10096-023-04551-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article
Senthakumaran, Thulasika
Moen, Aina E. F.
Tannæs, Tone M.
Endres, Alexander
Brackmann, Stephan A.
Rounge, Trine B.
Bemanian, Vahid
Tunsjø, Hege S.
Microbial dynamics with CRC progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls
title Microbial dynamics with CRC progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls
title_full Microbial dynamics with CRC progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls
title_fullStr Microbial dynamics with CRC progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls
title_full_unstemmed Microbial dynamics with CRC progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls
title_short Microbial dynamics with CRC progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls
title_sort microbial dynamics with crc progression: a study of the mucosal microbiota at multiple sites in cancers, adenomatous polyps, and healthy controls
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9899194/
https://www.ncbi.nlm.nih.gov/pubmed/36703031
http://dx.doi.org/10.1007/s10096-023-04551-7
work_keys_str_mv AT senthakumaranthulasika microbialdynamicswithcrcprogressionastudyofthemucosalmicrobiotaatmultiplesitesincancersadenomatouspolypsandhealthycontrols
AT moenainaef microbialdynamicswithcrcprogressionastudyofthemucosalmicrobiotaatmultiplesitesincancersadenomatouspolypsandhealthycontrols
AT tannæstonem microbialdynamicswithcrcprogressionastudyofthemucosalmicrobiotaatmultiplesitesincancersadenomatouspolypsandhealthycontrols
AT endresalexander microbialdynamicswithcrcprogressionastudyofthemucosalmicrobiotaatmultiplesitesincancersadenomatouspolypsandhealthycontrols
AT brackmannstephana microbialdynamicswithcrcprogressionastudyofthemucosalmicrobiotaatmultiplesitesincancersadenomatouspolypsandhealthycontrols
AT roungetrineb microbialdynamicswithcrcprogressionastudyofthemucosalmicrobiotaatmultiplesitesincancersadenomatouspolypsandhealthycontrols
AT bemanianvahid microbialdynamicswithcrcprogressionastudyofthemucosalmicrobiotaatmultiplesitesincancersadenomatouspolypsandhealthycontrols
AT tunsjøheges microbialdynamicswithcrcprogressionastudyofthemucosalmicrobiotaatmultiplesitesincancersadenomatouspolypsandhealthycontrols