Colonic microbiota is associated with inflammation and host epigenomic alterations in inflammatory bowel disease

F. J. Ryan; A. M. Ahern; R. S. Fitzgerald; E. J. Laserna-Mendieta; E. M. Power; A. G. Clooney; K. W. O’Donoghue; P. J. McMurdie; S. Iwai; A. Crits-Christoph; D. Sheehan; C. Moran; B. Flemer; A. L. Zomer; A. Fanning; J. O’Callaghan; J. Walton; A. Temko; W. Stack; L. Jackson; S. A. Joyce; S. Melgar; T. Z. DeSantis; J. T. Bell; F. Shanahan; M. J. Claesson

doi:10.1038/s41467-020-15342-5

Colonic microbiota is associated with inflammation and host epigenomic alterations in inflammatory bowel disease

F. J. Ryan, A. M. Ahern, R. S. Fitzgerald, E. J. Laserna-Mendieta, E. M. Power, A. G. Clooney, K. W. O’Donoghue, P. J. McMurdie, S. Iwai, A. Crits-Christoph, D. Sheehan, C. Moran, B. Flemer, A. L. Zomer, A. Fanning, J. O’Callaghan, J. Walton, A. Temko, W. Stack, L. JacksonS. A. Joyce, S. Melgar, T. Z. DeSantis, J. T. Bell, F. Shanahan, M. J. Claesson

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Abstract

Studies of inflammatory bowel disease (IBD) have been inconclusive in relating microbiota with distribution of inflammation. We report microbiota, host transcriptomics, epigenomics and genetics from matched inflamed and non-inflamed colonic mucosa [50 Crohn’s disease (CD); 80 ulcerative colitis (UC); 31 controls]. Changes in community-wide and within-patient microbiota are linked with inflammation, but we find no evidence for a distinct microbial diagnostic signature, probably due to heterogeneous host-microbe interactions, and show only marginal microbiota associations with habitual diet. Epithelial DNA methylation improves disease classification and is associated with both inflammation and microbiota composition. Microbiota sub-groups are driven by dominant Enterbacteriaceae and Bacteroides species, representative strains of which are pro-inflammatory in vitro, are also associated with immune-related epigenetic markers. In conclusion, inflamed and non-inflamed colonic segments in both CD and UC differ in microbiota composition and epigenetic profiles.

Original language	English
Article number	1512
Number of pages	12
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-15342-5
Publication status	Published - 23 Mar 2020
Externally published	Yes

Keywords

Data processing
Epigenomics
inflammatory bowel disease

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Ryan, F. J., Ahern, A. M., Fitzgerald, R. S., Laserna-Mendieta, E. J., Power, E. M., Clooney, A. G., O’Donoghue, K. W., McMurdie, P. J., Iwai, S., Crits-Christoph, A., Sheehan, D., Moran, C., Flemer, B., Zomer, A. L., Fanning, A., O’Callaghan, J., Walton, J., Temko, A., Stack, W., ... Claesson, M. J. (2020). Colonic microbiota is associated with inflammation and host epigenomic alterations in inflammatory bowel disease. Nature Communications, 11(1), Article 1512. https://doi.org/10.1038/s41467-020-15342-5

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title = "Colonic microbiota is associated with inflammation and host epigenomic alterations in inflammatory bowel disease",

abstract = "Studies of inflammatory bowel disease (IBD) have been inconclusive in relating microbiota with distribution of inflammation. We report microbiota, host transcriptomics, epigenomics and genetics from matched inflamed and non-inflamed colonic mucosa [50 Crohn{\textquoteright}s disease (CD); 80 ulcerative colitis (UC); 31 controls]. Changes in community-wide and within-patient microbiota are linked with inflammation, but we find no evidence for a distinct microbial diagnostic signature, probably due to heterogeneous host-microbe interactions, and show only marginal microbiota associations with habitual diet. Epithelial DNA methylation improves disease classification and is associated with both inflammation and microbiota composition. Microbiota sub-groups are driven by dominant Enterbacteriaceae and Bacteroides species, representative strains of which are pro-inflammatory in vitro, are also associated with immune-related epigenetic markers. In conclusion, inflamed and non-inflamed colonic segments in both CD and UC differ in microbiota composition and epigenetic profiles.",

keywords = "Data processing, Epigenomics, inflammatory bowel disease",

author = "Ryan, {F. J.} and Ahern, {A. M.} and Fitzgerald, {R. S.} and Laserna-Mendieta, {E. J.} and Power, {E. M.} and Clooney, {A. G.} and O{\textquoteright}Donoghue, {K. W.} and McMurdie, {P. J.} and S. Iwai and A. Crits-Christoph and D. Sheehan and C. Moran and B. Flemer and Zomer, {A. L.} and A. Fanning and J. O{\textquoteright}Callaghan and J. Walton and A. Temko and W. Stack and L. Jackson and Joyce, {S. A.} and S. Melgar and DeSantis, {T. Z.} and Bell, {J. T.} and F. Shanahan and Claesson, {M. J.}",

year = "2020",

month = mar,

day = "23",

doi = "10.1038/s41467-020-15342-5",

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Ryan, FJ, Ahern, AM, Fitzgerald, RS, Laserna-Mendieta, EJ, Power, EM, Clooney, AG, O’Donoghue, KW, McMurdie, PJ, Iwai, S, Crits-Christoph, A, Sheehan, D, Moran, C, Flemer, B, Zomer, AL, Fanning, A, O’Callaghan, J, Walton, J, Temko, A, Stack, W, Jackson, L, Joyce, SA, Melgar, S, DeSantis, TZ, Bell, JT, Shanahan, F & Claesson, MJ 2020, 'Colonic microbiota is associated with inflammation and host epigenomic alterations in inflammatory bowel disease', Nature Communications, vol. 11, no. 1, 1512. https://doi.org/10.1038/s41467-020-15342-5

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AU - Ryan, F. J.

AU - Ahern, A. M.

AU - Fitzgerald, R. S.

AU - Laserna-Mendieta, E. J.

AU - Power, E. M.

AU - Clooney, A. G.

AU - O’Donoghue, K. W.

AU - McMurdie, P. J.

AU - Iwai, S.

AU - Crits-Christoph, A.

AU - Sheehan, D.

AU - Moran, C.

AU - Flemer, B.

AU - Zomer, A. L.

AU - Fanning, A.

AU - O’Callaghan, J.

AU - Walton, J.

AU - Temko, A.

AU - Stack, W.

AU - Jackson, L.

AU - Joyce, S. A.

AU - Melgar, S.

AU - DeSantis, T. Z.

AU - Bell, J. T.

AU - Shanahan, F.

AU - Claesson, M. J.

PY - 2020/3/23

Y1 - 2020/3/23

N2 - Studies of inflammatory bowel disease (IBD) have been inconclusive in relating microbiota with distribution of inflammation. We report microbiota, host transcriptomics, epigenomics and genetics from matched inflamed and non-inflamed colonic mucosa [50 Crohn’s disease (CD); 80 ulcerative colitis (UC); 31 controls]. Changes in community-wide and within-patient microbiota are linked with inflammation, but we find no evidence for a distinct microbial diagnostic signature, probably due to heterogeneous host-microbe interactions, and show only marginal microbiota associations with habitual diet. Epithelial DNA methylation improves disease classification and is associated with both inflammation and microbiota composition. Microbiota sub-groups are driven by dominant Enterbacteriaceae and Bacteroides species, representative strains of which are pro-inflammatory in vitro, are also associated with immune-related epigenetic markers. In conclusion, inflamed and non-inflamed colonic segments in both CD and UC differ in microbiota composition and epigenetic profiles.

AB - Studies of inflammatory bowel disease (IBD) have been inconclusive in relating microbiota with distribution of inflammation. We report microbiota, host transcriptomics, epigenomics and genetics from matched inflamed and non-inflamed colonic mucosa [50 Crohn’s disease (CD); 80 ulcerative colitis (UC); 31 controls]. Changes in community-wide and within-patient microbiota are linked with inflammation, but we find no evidence for a distinct microbial diagnostic signature, probably due to heterogeneous host-microbe interactions, and show only marginal microbiota associations with habitual diet. Epithelial DNA methylation improves disease classification and is associated with both inflammation and microbiota composition. Microbiota sub-groups are driven by dominant Enterbacteriaceae and Bacteroides species, representative strains of which are pro-inflammatory in vitro, are also associated with immune-related epigenetic markers. In conclusion, inflamed and non-inflamed colonic segments in both CD and UC differ in microbiota composition and epigenetic profiles.

KW - Data processing

KW - Epigenomics

KW - inflammatory bowel disease

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DO - 10.1038/s41467-020-15342-5

M3 - Article

C2 - 32251296

AN - SCOPUS:85082529843

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 1512

ER -

Colonic microbiota is associated with inflammation and host epigenomic alterations in inflammatory bowel disease

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Keywords

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