The gut microbiota composition in patients with right- and left-sided colorectal cancer and after curative colectomy, as analyzed by 16S rRNA gene amplicon sequencing

Abstract Background Gut pathological microbial imbalance or dysbiosis is closely associated with colorectal cancer. Although there are observable differences in molecular and clinical characteristics between patients with right- and left-sided colon cancer, differences in their gut microbiomes have...

Full description

Bibliographic Details
Main Authors: Daisuke Suga, Hiroki Mizutani, Shunsuke Fukui, Mayu Kobayashi, Yasuaki Shimada, Yuuichi Nakazawa, Yuuki Nishiura, Yuuya Kawasaki, Isao Moritani, Yutaka Yamanaka, Hidekazu Inoue, Eiki Ojima, Yasuhiko Mohri, Hayato Nakagawa, Kaoru Dohi, Kei Takaba, Hideo Wada, Katsuya Shiraki
Format: Article
Language:English
Published: BMC 2022-06-01
Series:BMC Gastroenterology
Subjects:
Online Access:https://doi.org/10.1186/s12876-022-02382-y
_version_ 1811235666537742336
author Daisuke Suga
Hiroki Mizutani
Shunsuke Fukui
Mayu Kobayashi
Yasuaki Shimada
Yuuichi Nakazawa
Yuuki Nishiura
Yuuya Kawasaki
Isao Moritani
Yutaka Yamanaka
Hidekazu Inoue
Eiki Ojima
Yasuhiko Mohri
Hayato Nakagawa
Kaoru Dohi
Kei Takaba
Hideo Wada
Katsuya Shiraki
author_facet Daisuke Suga
Hiroki Mizutani
Shunsuke Fukui
Mayu Kobayashi
Yasuaki Shimada
Yuuichi Nakazawa
Yuuki Nishiura
Yuuya Kawasaki
Isao Moritani
Yutaka Yamanaka
Hidekazu Inoue
Eiki Ojima
Yasuhiko Mohri
Hayato Nakagawa
Kaoru Dohi
Kei Takaba
Hideo Wada
Katsuya Shiraki
author_sort Daisuke Suga
collection DOAJ
description Abstract Background Gut pathological microbial imbalance or dysbiosis is closely associated with colorectal cancer. Although there are observable differences in molecular and clinical characteristics between patients with right- and left-sided colon cancer, differences in their gut microbiomes have not been thoroughly investigated. Furthermore, subsequent changes in microbiota status after partial colectomy remain unknown. We examined the human gut microbiota composition to determine its relationship with colon cancer and partial colon resection according to location. Methods Stool samples from forty-one subjects (10 in the control group, 10 in the right-sided colon cancer [RCC] group, 6 in the sigmoid colon cancer [SCC] group, 9 in the right colon resection [RCR] group and 6 in the sigmoid colon resection [SCR] group) were collected, and DNA was extracted. After terminal restriction fragment length polymorphism (T-RFLP) analysis, the samples were subjected to 16S rRNA gene amplicon sequencing, and the metabolic function of the microbiota was predicted using PICRUSt2. Results T-RFLP analysis showed a reduced ratio of clostridial cluster XIVa in the SCC patients and clostridial cluster IX in the RCC patients, although these changes were not evident in the RCR or SCR patients. 16S rRNA gene amplicon sequencing demonstrated that the diversity of the gut microbiota in the RCC group was higher than that in the control group, and the diversity in the SCR group was significantly higher than that in the RCR group. Principal coordinate analysis (PCoA) revealed significant differences according to the group. Analyses of the microbiota revealed that Firmicutes was significantly dominant in the RCC group and that the SCC group had a higher abundance of Verrucomicrobia. At the genus level, linear discriminant analysis effect size (LEfSe) revealed several bacteria, such as Ruminococcaceae, Streptococcaceae, Clostridiaceae, Gemellaceae, and Desulfovibrio, in the RCC group and several oral microbiomes in the SCC group. Metabolic function prediction revealed that cholesterol transport- and metabolism-related enzymes were specifically upregulated in the RCC group and that cobalamin metabolism-related enzymes were downregulated in the SCC group. Conclusion Gut microbial properties differ between RCC and SCC patients and between right hemicolectomy and sigmoidectomy patients and may contribute to clinical manifestations.
first_indexed 2024-04-12T11:55:54Z
format Article
id doaj.art-5edae0560d5b458b9887178703df1910
institution Directory Open Access Journal
issn 1471-230X
language English
last_indexed 2024-04-12T11:55:54Z
publishDate 2022-06-01
publisher BMC
record_format Article
series BMC Gastroenterology
spelling doaj.art-5edae0560d5b458b9887178703df19102022-12-22T03:34:00ZengBMCBMC Gastroenterology1471-230X2022-06-0122111310.1186/s12876-022-02382-yThe gut microbiota composition in patients with right- and left-sided colorectal cancer and after curative colectomy, as analyzed by 16S rRNA gene amplicon sequencingDaisuke Suga0Hiroki Mizutani1Shunsuke Fukui2Mayu Kobayashi3Yasuaki Shimada4Yuuichi Nakazawa5Yuuki Nishiura6Yuuya Kawasaki7Isao Moritani8Yutaka Yamanaka9Hidekazu Inoue10Eiki Ojima11Yasuhiko Mohri12Hayato Nakagawa13Kaoru Dohi14Kei Takaba15Hideo Wada16Katsuya Shiraki17Department of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterDepartment of Surgery, Mie General Medical CenterDepartment of Surgery, Mie General Medical CenterDepartment of Gastroenterology, Mie University Graduate School of MedicineDepartment of Cardiology and Nephrology, Mie University Graduate School of MedicineDepartment of Research Center, Mie General Medical CenterDepartment of Research Center, Mie General Medical CenterDepartment of Gastroenterology, Mie General Medical CenterAbstract Background Gut pathological microbial imbalance or dysbiosis is closely associated with colorectal cancer. Although there are observable differences in molecular and clinical characteristics between patients with right- and left-sided colon cancer, differences in their gut microbiomes have not been thoroughly investigated. Furthermore, subsequent changes in microbiota status after partial colectomy remain unknown. We examined the human gut microbiota composition to determine its relationship with colon cancer and partial colon resection according to location. Methods Stool samples from forty-one subjects (10 in the control group, 10 in the right-sided colon cancer [RCC] group, 6 in the sigmoid colon cancer [SCC] group, 9 in the right colon resection [RCR] group and 6 in the sigmoid colon resection [SCR] group) were collected, and DNA was extracted. After terminal restriction fragment length polymorphism (T-RFLP) analysis, the samples were subjected to 16S rRNA gene amplicon sequencing, and the metabolic function of the microbiota was predicted using PICRUSt2. Results T-RFLP analysis showed a reduced ratio of clostridial cluster XIVa in the SCC patients and clostridial cluster IX in the RCC patients, although these changes were not evident in the RCR or SCR patients. 16S rRNA gene amplicon sequencing demonstrated that the diversity of the gut microbiota in the RCC group was higher than that in the control group, and the diversity in the SCR group was significantly higher than that in the RCR group. Principal coordinate analysis (PCoA) revealed significant differences according to the group. Analyses of the microbiota revealed that Firmicutes was significantly dominant in the RCC group and that the SCC group had a higher abundance of Verrucomicrobia. At the genus level, linear discriminant analysis effect size (LEfSe) revealed several bacteria, such as Ruminococcaceae, Streptococcaceae, Clostridiaceae, Gemellaceae, and Desulfovibrio, in the RCC group and several oral microbiomes in the SCC group. Metabolic function prediction revealed that cholesterol transport- and metabolism-related enzymes were specifically upregulated in the RCC group and that cobalamin metabolism-related enzymes were downregulated in the SCC group. Conclusion Gut microbial properties differ between RCC and SCC patients and between right hemicolectomy and sigmoidectomy patients and may contribute to clinical manifestations.https://doi.org/10.1186/s12876-022-02382-yColon cancerMicrobiotaT-RFLP16S rRNA gene amplicon sequencing
spellingShingle Daisuke Suga
Hiroki Mizutani
Shunsuke Fukui
Mayu Kobayashi
Yasuaki Shimada
Yuuichi Nakazawa
Yuuki Nishiura
Yuuya Kawasaki
Isao Moritani
Yutaka Yamanaka
Hidekazu Inoue
Eiki Ojima
Yasuhiko Mohri
Hayato Nakagawa
Kaoru Dohi
Kei Takaba
Hideo Wada
Katsuya Shiraki
The gut microbiota composition in patients with right- and left-sided colorectal cancer and after curative colectomy, as analyzed by 16S rRNA gene amplicon sequencing
BMC Gastroenterology
Colon cancer
Microbiota
T-RFLP
16S rRNA gene amplicon sequencing
title The gut microbiota composition in patients with right- and left-sided colorectal cancer and after curative colectomy, as analyzed by 16S rRNA gene amplicon sequencing
title_full The gut microbiota composition in patients with right- and left-sided colorectal cancer and after curative colectomy, as analyzed by 16S rRNA gene amplicon sequencing
title_fullStr The gut microbiota composition in patients with right- and left-sided colorectal cancer and after curative colectomy, as analyzed by 16S rRNA gene amplicon sequencing
title_full_unstemmed The gut microbiota composition in patients with right- and left-sided colorectal cancer and after curative colectomy, as analyzed by 16S rRNA gene amplicon sequencing
title_short The gut microbiota composition in patients with right- and left-sided colorectal cancer and after curative colectomy, as analyzed by 16S rRNA gene amplicon sequencing
title_sort gut microbiota composition in patients with right and left sided colorectal cancer and after curative colectomy as analyzed by 16s rrna gene amplicon sequencing
topic Colon cancer
Microbiota
T-RFLP
16S rRNA gene amplicon sequencing
url https://doi.org/10.1186/s12876-022-02382-y
work_keys_str_mv AT daisukesuga thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT hirokimizutani thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT shunsukefukui thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT mayukobayashi thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yasuakishimada thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yuuichinakazawa thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yuukinishiura thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yuuyakawasaki thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT isaomoritani thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yutakayamanaka thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT hidekazuinoue thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT eikiojima thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yasuhikomohri thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT hayatonakagawa thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT kaorudohi thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT keitakaba thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT hideowada thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT katsuyashiraki thegutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT daisukesuga gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT hirokimizutani gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT shunsukefukui gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT mayukobayashi gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yasuakishimada gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yuuichinakazawa gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yuukinishiura gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yuuyakawasaki gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT isaomoritani gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yutakayamanaka gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT hidekazuinoue gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT eikiojima gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT yasuhikomohri gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT hayatonakagawa gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT kaorudohi gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT keitakaba gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT hideowada gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing
AT katsuyashiraki gutmicrobiotacompositioninpatientswithrightandleftsidedcolorectalcancerandaftercurativecolectomyasanalyzedby16srrnageneampliconsequencing