Skip to main content
Top
Published in: Gut Pathogens 1/2021

01-12-2021 | Respiratory Microbiota | Research

Bacteroides, butyric acid and t10,c12-CLA changes in colorectal adenomatous polyp patients

Authors: Ciyan Chen, Min Niu, Junxi Pan, Na Du, Shumin Liu, Huanqin Li, Qiuyue He, Jian Mao, Yong Duan, Yan Du

Published in: Gut Pathogens | Issue 1/2021

Login to get access

Abstract

Background

Colorectal adenomatous polyps (CAPs) are considered precancerous lesions of colorectal cancer (CRC). The gut microbiota participates in the process of digestion and, in the process, produces metabolites, mainly short-chain fatty acids (SCFAs), secondary bile acids and conjugated linoleic acid (CLA). This study aimed to investigate the gut microbiota constituents and metabolites in the faeces of CAP patients to identify microbiota or metabolites that can be used as sensitive biological predictors and to provide a theoretical basis for the clinical treatment of CAPs.

Methods

16S rRNA sequence analysis was used to detect microbial changes in the faeces of CAP patients. qPCR analysis was used to evaluate the ability of the microbiota to produce metabolites, and the contents of metabolites in faeces were detected by ion chromatography and ultra-performance liquid chromatography-tandem mass spectrometry (UPLC-MS/MS).

Results

Based on the detection of the gut microbiota, patients with CAPs had increased abundances of Bacteroides and Citrobacter, and the abundances of Weissella and Lactobacillus were decreased. We also explored gene expression, and the abundance of butyrate-producing bacterial genes was significantly increased in the faeces of CAP patients, but those of secondary bile acid-producing and CLA-producing bacterial genes showed no differences in faecal samples. The acetic acid and butyric acid contents were increased in the faeces of the CAP group, and the healthy control group had higher t10,c12-CLA contents.

Conclusion

The gut microbiota analysis results, assessed in faeces, showed that Bacteroides and Citrobacter were positively correlated with CAPs, which indicated that changes in specific genera might be detrimental to intestinal health. In addition, t10,c12-CLA played an important role in protecting the intestine.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.PubMed Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.PubMed
3.
go back to reference Feng Q, Liang S, Jia H, Stadlmayr A, Tang L, Lan Z, et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun. 2015;6:6528.PubMedCrossRef Feng Q, Liang S, Jia H, Stadlmayr A, Tang L, Lan Z, et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun. 2015;6:6528.PubMedCrossRef
4.
go back to reference Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opon Gastroenterol. 2015;31(1):69–75.CrossRef Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opon Gastroenterol. 2015;31(1):69–75.CrossRef
5.
go back to reference Katsuyoshi M, Takanori K. The gut microbiota and inflammatory bowel disease. Semin Immunopathol. 2015;37(1):47–55.CrossRef Katsuyoshi M, Takanori K. The gut microbiota and inflammatory bowel disease. Semin Immunopathol. 2015;37(1):47–55.CrossRef
7.
go back to reference Shen X, Miao J, Wan Q, Wang S, Li M, Pu F, et al. Possible correlation between gut microbiota and immunity among healthy middle-aged and elderly people in southwest China. Gut Pathog. 2018;10:4.PubMedPubMedCentralCrossRef Shen X, Miao J, Wan Q, Wang S, Li M, Pu F, et al. Possible correlation between gut microbiota and immunity among healthy middle-aged and elderly people in southwest China. Gut Pathog. 2018;10:4.PubMedPubMedCentralCrossRef
8.
go back to reference Tilg H, Adolph TE, Gerner RR, Moschen AR. The intestinal microbiota in colorectal cancer. Cancer Cell. 2018;33(6):954.PubMedCrossRef Tilg H, Adolph TE, Gerner RR, Moschen AR. The intestinal microbiota in colorectal cancer. Cancer Cell. 2018;33(6):954.PubMedCrossRef
10.
go back to reference Rajagopala SV, Vashee S, Oldfield LM, Suzuki Y, Venter JC, Telenti A, et al. The human microbiome and cancer. Cancer Prev Res. 2017;10(4):226–34.CrossRef Rajagopala SV, Vashee S, Oldfield LM, Suzuki Y, Venter JC, Telenti A, et al. The human microbiome and cancer. Cancer Prev Res. 2017;10(4):226–34.CrossRef
11.
go back to reference Yachida S, Mizutani S, Shiroma H, Shiba S, Nakajima T, Sakamoto T, et al. Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer. Nat Med. 2019;25(6):968–76.PubMedCrossRef Yachida S, Mizutani S, Shiroma H, Shiba S, Nakajima T, Sakamoto T, et al. Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer. Nat Med. 2019;25(6):968–76.PubMedCrossRef
12.
go back to reference Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol. 2014;12(10):661–72.PubMedCrossRef Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol. 2014;12(10):661–72.PubMedCrossRef
13.
go back to reference Degen C, Habermann N, Piegholdt S, Glei M, Jahreis G. Human colon cell culture models of different transformation stages to assess conjugated linoleic acid and conjugated linolenic acid metabolism: challenges and chances. Toxicol In Vitro. 2012;26(6):985–92.PubMedCrossRef Degen C, Habermann N, Piegholdt S, Glei M, Jahreis G. Human colon cell culture models of different transformation stages to assess conjugated linoleic acid and conjugated linolenic acid metabolism: challenges and chances. Toxicol In Vitro. 2012;26(6):985–92.PubMedCrossRef
14.
go back to reference Graf D, Di Cagno R, Fak F, Flint HJ, Nyman M, Saarela M, et al. Contribution of diet to the composition of the human gut microbiota. Microb Ecol Health Dis. 2015;26:26164.PubMed Graf D, Di Cagno R, Fak F, Flint HJ, Nyman M, Saarela M, et al. Contribution of diet to the composition of the human gut microbiota. Microb Ecol Health Dis. 2015;26:26164.PubMed
15.
go back to reference Sun HD, Jiang ZY. Recent progress in gut microbiota and bile acid metabolism. Chin Bull Life Sci. 2016;28:1405–9. Sun HD, Jiang ZY. Recent progress in gut microbiota and bile acid metabolism. Chin Bull Life Sci. 2016;28:1405–9.
16.
go back to reference Yadav M, Verma MK, Chauhan NS. A review of metabolic potential of human gut microbiome in human nutrition. Arch Microbiol. 2018;200(2):203–17.PubMedCrossRef Yadav M, Verma MK, Chauhan NS. A review of metabolic potential of human gut microbiome in human nutrition. Arch Microbiol. 2018;200(2):203–17.PubMedCrossRef
17.
go back to reference Davenport JR, Su T, Zhao Z, Coleman HG, Smalley WE, Ness RM, et al. Modifiable lifestyle factors associated with risk of sessile serrated polyps, conventional adenomas and hyperplastic polyps. Gut. 2016;67(3):456.PubMedCrossRef Davenport JR, Su T, Zhao Z, Coleman HG, Smalley WE, Ness RM, et al. Modifiable lifestyle factors associated with risk of sessile serrated polyps, conventional adenomas and hyperplastic polyps. Gut. 2016;67(3):456.PubMedCrossRef
19.
go back to reference Thomas AM, Jesus EC, Lopes A, Aguiar A Jr, Begnami MD, Rocha RM, et al. Tissue-associated bacterial alterations in rectal carcinoma patients revealed by 16S rRNA community profiling. Front Cell Infect Microbiol. 2016;6:179.PubMedPubMedCentralCrossRef Thomas AM, Jesus EC, Lopes A, Aguiar A Jr, Begnami MD, Rocha RM, et al. Tissue-associated bacterial alterations in rectal carcinoma patients revealed by 16S rRNA community profiling. Front Cell Infect Microbiol. 2016;6:179.PubMedPubMedCentralCrossRef
20.
go back to reference Flemer B, Lynch DB, Brown JM, Jeffery IB, Ryan FJ, Claesson MJ, et al. Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut. 2017;66(4):633–43.PubMedCrossRef Flemer B, Lynch DB, Brown JM, Jeffery IB, Ryan FJ, Claesson MJ, et al. Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut. 2017;66(4):633–43.PubMedCrossRef
21.
go back to reference Gao Z, Guo B, Gao R, Zhu Q, Qin H. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol. 2015;6:20.PubMedPubMedCentral Gao Z, Guo B, Gao R, Zhu Q, Qin H. Microbiota disbiosis is associated with colorectal cancer. Front Microbiol. 2015;6:20.PubMedPubMedCentral
22.
go back to reference Wu N, Yang X, Zhang R, Li J, Xiao X, Hu Y, et al. Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol. 2013;66(2):462–70.PubMedCrossRef Wu N, Yang X, Zhang R, Li J, Xiao X, Hu Y, et al. Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol. 2013;66(2):462–70.PubMedCrossRef
23.
24.
go back to reference Flanagan L, Schmid J, Ebert M, Soucek P, Kunicka T, Liska V, et al. Fusobacterium nucleatumassociates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. Eur J Clin Microbiol Infect Dis. 2014;33(8):1381–90.PubMedCrossRef Flanagan L, Schmid J, Ebert M, Soucek P, Kunicka T, Liska V, et al. Fusobacterium nucleatumassociates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. Eur J Clin Microbiol Infect Dis. 2014;33(8):1381–90.PubMedCrossRef
25.
go back to reference Marks P, Richon VM, Rifkind RA. Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J Natl Cancer Inst. 2000;92(15):1210–6.PubMedCrossRef Marks P, Richon VM, Rifkind RA. Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J Natl Cancer Inst. 2000;92(15):1210–6.PubMedCrossRef
27.
go back to reference Belcheva A, Irrazabal T, Robertson Susan J, Streutker C, Maughan H, Rubino S, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell. 2014;158(2):288–99.PubMedCrossRef Belcheva A, Irrazabal T, Robertson Susan J, Streutker C, Maughan H, Rubino S, et al. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell. 2014;158(2):288–99.PubMedCrossRef
28.
go back to reference Ferrer-Picon E, Dotti I, Corraliza AM, Mayorgas A, Esteller M, Perales JC, et al. Intestinal inflammation modulates the epithelial response to butyrate in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2020;26(1):43–55.PubMedCrossRef Ferrer-Picon E, Dotti I, Corraliza AM, Mayorgas A, Esteller M, Perales JC, et al. Intestinal inflammation modulates the epithelial response to butyrate in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2020;26(1):43–55.PubMedCrossRef
29.
go back to reference Chen H, Yu Y, Wang J, Lin Y, Kong X, Yang C, et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr. 2013;97(5):1044–52.PubMedCrossRef Chen H, Yu Y, Wang J, Lin Y, Kong X, Yang C, et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr. 2013;97(5):1044–52.PubMedCrossRef
30.
go back to reference Keku TO, Dulal S, Deveaux A, Jovov B, Han X. The gastrointestinal microbiota and colorectal cancer. Am J Physiol Gastrointest Liver Physiol. 2015;308(5):G351.PubMedCrossRef Keku TO, Dulal S, Deveaux A, Jovov B, Han X. The gastrointestinal microbiota and colorectal cancer. Am J Physiol Gastrointest Liver Physiol. 2015;308(5):G351.PubMedCrossRef
31.
go back to reference Reiser R. The biochemical conversions of conjugated dienoic and trienoic fatty acids. Arch Biochem Biophys. 1951;32(1):113–20.PubMedCrossRef Reiser R. The biochemical conversions of conjugated dienoic and trienoic fatty acids. Arch Biochem Biophys. 1951;32(1):113–20.PubMedCrossRef
32.
go back to reference Li K, Zhou N, Li HY, Wang L. Physiological function for conjugated linoleic acid. Food Res Dev. 2012;33:226–8.CrossRef Li K, Zhou N, Li HY, Wang L. Physiological function for conjugated linoleic acid. Food Res Dev. 2012;33:226–8.CrossRef
33.
go back to reference Torre AD, Debiton E, Durand D, Chardigny JM, Berdeaux O, Loreau O, et al. Conjugated linoleic acid isomers and their conjugated derivatives inhibit growth of human cancer cell lines. Anticancer Res. 2005;25(6B):3943–9.PubMed Torre AD, Debiton E, Durand D, Chardigny JM, Berdeaux O, Loreau O, et al. Conjugated linoleic acid isomers and their conjugated derivatives inhibit growth of human cancer cell lines. Anticancer Res. 2005;25(6B):3943–9.PubMed
34.
go back to reference Tanmahasamut P, Liu J, Hendry LB, Sidell N. Conjugated linoleic acid blocks estrogen signaling in human breast cancer cells. J Nutr. 2004;134(3):674.PubMedCrossRef Tanmahasamut P, Liu J, Hendry LB, Sidell N. Conjugated linoleic acid blocks estrogen signaling in human breast cancer cells. J Nutr. 2004;134(3):674.PubMedCrossRef
35.
go back to reference Cho HJ, Kim EJ, Lim SS, Kim MK, Sung M-K, Kim J-S, et al. Trans-10, cis-12, not cis-9, trans-11, conjugated linoleic acid inhibits G1-S progression in HT-29 human colon cancer cells. J Nutr. 2006;136(4):893–8.PubMedCrossRef Cho HJ, Kim EJ, Lim SS, Kim MK, Sung M-K, Kim J-S, et al. Trans-10, cis-12, not cis-9, trans-11, conjugated linoleic acid inhibits G1-S progression in HT-29 human colon cancer cells. J Nutr. 2006;136(4):893–8.PubMedCrossRef
36.
go back to reference Raimondi S, Amaretti A, Leonardi A, Quartieri A, Gozzoli C, Rossi M. Conjugated linoleic acid production by bifidobacteria: screening, kinetic, and composition. BioMed Res Int. 2016;2016(6):1–8. Raimondi S, Amaretti A, Leonardi A, Quartieri A, Gozzoli C, Rossi M. Conjugated linoleic acid production by bifidobacteria: screening, kinetic, and composition. BioMed Res Int. 2016;2016(6):1–8.
37.
go back to reference Cao H, Xu M, Dong W, Deng B, Wang S, Zhang Y, et al. Secondary bile acid-induced dysbiosis promotes intestinal carcinogenesis. Int J Cancer. 2017;140(11):2545–56.PubMedCrossRef Cao H, Xu M, Dong W, Deng B, Wang S, Zhang Y, et al. Secondary bile acid-induced dysbiosis promotes intestinal carcinogenesis. Int J Cancer. 2017;140(11):2545–56.PubMedCrossRef
38.
go back to reference Tong JL, Ran ZH, Shen J, Fan GQ, Xiao SD. Association between fecal bile acids and colorectal cancer: a meta-analysis of observational studies. Yonsei Med J. 2008;49(5):792.PubMedPubMedCentralCrossRef Tong JL, Ran ZH, Shen J, Fan GQ, Xiao SD. Association between fecal bile acids and colorectal cancer: a meta-analysis of observational studies. Yonsei Med J. 2008;49(5):792.PubMedPubMedCentralCrossRef
39.
go back to reference Feng H-Y, Chen Y-C. Role of bile acids in carcinogenesis of pancreatic cancer: an old topic with new perspective. World J Gastroenterol. 2016;22(33):7463–77.PubMedPubMedCentralCrossRef Feng H-Y, Chen Y-C. Role of bile acids in carcinogenesis of pancreatic cancer: an old topic with new perspective. World J Gastroenterol. 2016;22(33):7463–77.PubMedPubMedCentralCrossRef
40.
go back to reference Zheng X, Huang F, Zhao A, Lei S, Zhang Y, Xie G, et al. Bile acid is a significant host factor shaping the gut microbiome of diet-induced obese mice. BMC Biol. 2017;15(1):120.PubMedPubMedCentralCrossRef Zheng X, Huang F, Zhao A, Lei S, Zhang Y, Xie G, et al. Bile acid is a significant host factor shaping the gut microbiome of diet-induced obese mice. BMC Biol. 2017;15(1):120.PubMedPubMedCentralCrossRef
41.
go back to reference Ruengsomwong S, La-Ongkham O, Jiang J, Wannissorn B, Nakayama J, Nitisinprasert S. Microbial community of healthy Thai vegetarians and non-vegetarians, their core gut microbiota, and pathogen risk. J Microbiol Biotechnol. 2016;26(10):1723–35.PubMedCrossRef Ruengsomwong S, La-Ongkham O, Jiang J, Wannissorn B, Nakayama J, Nitisinprasert S. Microbial community of healthy Thai vegetarians and non-vegetarians, their core gut microbiota, and pathogen risk. J Microbiol Biotechnol. 2016;26(10):1723–35.PubMedCrossRef
42.
go back to reference Mullish BH, Pechlivanis A, Barker GF, Thursz MR, Marchesi JR, McDonald JAK. Functional microbiomics: evaluation of gut microbiota-bile acid metabolism interactions in health and disease. Methods. 2018;149:49–58.PubMedPubMedCentralCrossRef Mullish BH, Pechlivanis A, Barker GF, Thursz MR, Marchesi JR, McDonald JAK. Functional microbiomics: evaluation of gut microbiota-bile acid metabolism interactions in health and disease. Methods. 2018;149:49–58.PubMedPubMedCentralCrossRef
44.
go back to reference Brunkwall L, Orho-Melander M. The gut microbiome as a target for prevention and treatment of hyperglycaemia in type 2 diabetes: from current human evidence to future possibilities. Diabetologia. 2017;60(6):943–51.PubMedPubMedCentralCrossRef Brunkwall L, Orho-Melander M. The gut microbiome as a target for prevention and treatment of hyperglycaemia in type 2 diabetes: from current human evidence to future possibilities. Diabetologia. 2017;60(6):943–51.PubMedPubMedCentralCrossRef
45.
46.
go back to reference Kitai T, Tang WHW. Gut microbiota in cardiovascular disease and heart failure. Clin Sci. 2018;132(1):85–91.CrossRef Kitai T, Tang WHW. Gut microbiota in cardiovascular disease and heart failure. Clin Sci. 2018;132(1):85–91.CrossRef
48.
go back to reference Malan-Muller S, Valles-Colomer M, Raes J, Lowry CA, Seedat S, Hemmings SMJ. The gut microbiome and mental health: implications for anxiety- and trauma-related disorders. OMICS. 2018;22(2):90–107.PubMedCrossRef Malan-Muller S, Valles-Colomer M, Raes J, Lowry CA, Seedat S, Hemmings SMJ. The gut microbiome and mental health: implications for anxiety- and trauma-related disorders. OMICS. 2018;22(2):90–107.PubMedCrossRef
49.
go back to reference Wong SH, Kwong TNY, Wu CY, Yu J. Clinical applications of gut microbiota in cancer biology. Semin Cancer Biol. 2019;55:28–36.PubMedCrossRef Wong SH, Kwong TNY, Wu CY, Yu J. Clinical applications of gut microbiota in cancer biology. Semin Cancer Biol. 2019;55:28–36.PubMedCrossRef
Metadata
Title
Bacteroides, butyric acid and t10,c12-CLA changes in colorectal adenomatous polyp patients
Authors
Ciyan Chen
Min Niu
Junxi Pan
Na Du
Shumin Liu
Huanqin Li
Qiuyue He
Jian Mao
Yong Duan
Yan Du
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2021
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-020-00395-0

Other articles of this Issue 1/2021

Gut Pathogens 1/2021 Go to the issue