Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients

ABSTRACT We have previously identified a crypt-specific core microbiota (CSCM) in the colons of healthy laboratory mice and related wild rodents. Here, we confirm that a CSCM also exists in the human colon and appears to be altered during colon cancer. The colonic microbiota is suggested to be invol...

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Autores principales: Azadeh Saffarian, Céline Mulet, Béatrice Regnault, Aurélien Amiot, Jeanne Tran-Van-Nhieu, Jacques Ravel, Iradj Sobhani, Philippe J. Sansonetti, Thierry Pédron
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:a9487f327aa04ae2af265cda1c0154a82021-11-15T16:22:09ZCrypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients10.1128/mBio.01315-192150-7511https://doaj.org/article/a9487f327aa04ae2af265cda1c0154a82019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01315-19https://doaj.org/toc/2150-7511ABSTRACT We have previously identified a crypt-specific core microbiota (CSCM) in the colons of healthy laboratory mice and related wild rodents. Here, we confirm that a CSCM also exists in the human colon and appears to be altered during colon cancer. The colonic microbiota is suggested to be involved in the development of colorectal cancer (CRC). Because the microbiota identified in fecal samples from CRC patients does not directly reflect the microbiota associated with tumor tissues themselves, we sought to characterize the bacterial communities from the crypts and associated adjacent mucosal surfaces of 58 patients (tumor and normal homologous tissue) and 9 controls with normal colonoscopy results. Here, we confirm that bacteria colonize human colonic crypts in both control and CRC tissues, and using laser-microdissected tissues and 16S rRNA gene sequencing, we further show that right and left crypt- and mucosa-associated bacterial communities are significantly different. In addition to Bacteroidetes and Firmicutes, and as with murine proximal colon crypts, environmental nonfermentative Proteobacteria are found in human colonic crypts. Fusobacterium and Bacteroides fragilis are more abundant in right-side tumors, whereas Parvimonas micra is more prevalent in left-side tumors. More precisely, Fusobacterium periodonticum is more abundant in crypts from cancerous samples in the right colon than in associated nontumoral samples from adjacent areas but not in left-side colonic samples. Future analysis of the interaction between these bacteria and the crypt epithelium, particularly intestinal stem cells, will allow deciphering of their possible oncogenic potential. IMPORTANCE Due to the huge number of bacteria constituting the human colon microbiota, alteration in the balance of its constitutive taxa (i.e., dysbiosis) is highly suspected of being involved in colorectal oncogenesis. Indeed, bacterial signatures in association with CRC have been described. These signatures may vary if bacteria are identified in feces or in association with tumor tissues. Here, we show that bacteria colonize human colonic crypts in tissues obtained from patients with CRC and with normal colonoscopy results. Aerobic nonfermentative Proteobacteria previously identified as constitutive of the crypt-specific core microbiota in murine colonic samples are similarly prevalent in human colonic crypts in combination with other anaerobic taxa. We also show that bacterial signatures characterizing the crypts of colonic tumors vary depending whether right-side or left-side tumors are analyzed.Azadeh SaffarianCéline MuletBéatrice RegnaultAurélien AmiotJeanne Tran-Van-NhieuJacques RavelIradj SobhaniPhilippe J. SansonettiThierry PédronAmerican Society for Microbiologyarticlecolon cancerintestinal cryptsmicrobiotaMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution DOAJ
collection DOAJ
language EN
topic colon cancer
intestinal crypts
microbiota
Microbiology
QR1-502
spellingShingle colon cancer
intestinal crypts
microbiota
Microbiology
QR1-502
Azadeh Saffarian
Céline Mulet
Béatrice Regnault
Aurélien Amiot
Jeanne Tran-Van-Nhieu
Jacques Ravel
Iradj Sobhani
Philippe J. Sansonetti
Thierry Pédron
Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients
description ABSTRACT We have previously identified a crypt-specific core microbiota (CSCM) in the colons of healthy laboratory mice and related wild rodents. Here, we confirm that a CSCM also exists in the human colon and appears to be altered during colon cancer. The colonic microbiota is suggested to be involved in the development of colorectal cancer (CRC). Because the microbiota identified in fecal samples from CRC patients does not directly reflect the microbiota associated with tumor tissues themselves, we sought to characterize the bacterial communities from the crypts and associated adjacent mucosal surfaces of 58 patients (tumor and normal homologous tissue) and 9 controls with normal colonoscopy results. Here, we confirm that bacteria colonize human colonic crypts in both control and CRC tissues, and using laser-microdissected tissues and 16S rRNA gene sequencing, we further show that right and left crypt- and mucosa-associated bacterial communities are significantly different. In addition to Bacteroidetes and Firmicutes, and as with murine proximal colon crypts, environmental nonfermentative Proteobacteria are found in human colonic crypts. Fusobacterium and Bacteroides fragilis are more abundant in right-side tumors, whereas Parvimonas micra is more prevalent in left-side tumors. More precisely, Fusobacterium periodonticum is more abundant in crypts from cancerous samples in the right colon than in associated nontumoral samples from adjacent areas but not in left-side colonic samples. Future analysis of the interaction between these bacteria and the crypt epithelium, particularly intestinal stem cells, will allow deciphering of their possible oncogenic potential. IMPORTANCE Due to the huge number of bacteria constituting the human colon microbiota, alteration in the balance of its constitutive taxa (i.e., dysbiosis) is highly suspected of being involved in colorectal oncogenesis. Indeed, bacterial signatures in association with CRC have been described. These signatures may vary if bacteria are identified in feces or in association with tumor tissues. Here, we show that bacteria colonize human colonic crypts in tissues obtained from patients with CRC and with normal colonoscopy results. Aerobic nonfermentative Proteobacteria previously identified as constitutive of the crypt-specific core microbiota in murine colonic samples are similarly prevalent in human colonic crypts in combination with other anaerobic taxa. We also show that bacterial signatures characterizing the crypts of colonic tumors vary depending whether right-side or left-side tumors are analyzed.
format article
author Azadeh Saffarian
Céline Mulet
Béatrice Regnault
Aurélien Amiot
Jeanne Tran-Van-Nhieu
Jacques Ravel
Iradj Sobhani
Philippe J. Sansonetti
Thierry Pédron
author_facet Azadeh Saffarian
Céline Mulet
Béatrice Regnault
Aurélien Amiot
Jeanne Tran-Van-Nhieu
Jacques Ravel
Iradj Sobhani
Philippe J. Sansonetti
Thierry Pédron
author_sort Azadeh Saffarian
title Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients
title_short Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients
title_full Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients
title_fullStr Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients
title_full_unstemmed Crypt- and Mucosa-Associated Core Microbiotas in Humans and Their Alteration in Colon Cancer Patients
title_sort crypt- and mucosa-associated core microbiotas in humans and their alteration in colon cancer patients
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/a9487f327aa04ae2af265cda1c0154a8
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