Alterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypes

<p>Musculoskeletal diseases affect up to 20% of adults worldwide. The gut microbiome has been implicated in inflammatory conditions, but large-scale metagenomic evaluations have not yet traced the routes by which immunity in the gut affects inflammatory arthritis. To characterize the community...

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Main Authors: Thompson, KN, Bonham, KS, Ilott, NE, Colmenero, P, Bullers, SJ, Brough, I, Pearson, C, Moussa, C, Kumar, V, Lam, LH, Jackson, MA, Kiriakidis, S, Taylor, PC, Marsden, B, Bowness, P, Powrie, F
Other Authors: Inflammatory Arthritis Microbiome Consortium (IAMC) investigators group
Format: Journal article
Language:English
Published: American Association for the Advancement of Science 2023
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author Thompson, KN
Bonham, KS
Ilott, NE
Colmenero, P
Bullers, SJ
Brough, I
Pearson, C
Moussa, C
Kumar, V
Lam, LH
Jackson, MA
Kiriakidis, S
Taylor, PC
Marsden, B
Bowness, P
Powrie, F
author2 Inflammatory Arthritis Microbiome Consortium (IAMC) investigators group
author_facet Inflammatory Arthritis Microbiome Consortium (IAMC) investigators group
Thompson, KN
Bonham, KS
Ilott, NE
Colmenero, P
Bullers, SJ
Brough, I
Pearson, C
Moussa, C
Kumar, V
Lam, LH
Jackson, MA
Kiriakidis, S
Taylor, PC
Marsden, B
Bowness, P
Powrie, F
author_sort Thompson, KN
collection OXFORD
description <p>Musculoskeletal diseases affect up to 20% of adults worldwide. The gut microbiome has been implicated in inflammatory conditions, but large-scale metagenomic evaluations have not yet traced the routes by which immunity in the gut affects inflammatory arthritis. To characterize the community structure and associated functional processes driving gut microbial involvement in arthritis, the Inflammatory Arthritis Microbiome Consortium investigated 440 stool shotgun metagenomes comprising 221 adults diagnosed with rheumatoid arthritis, ankylosing spondylitis, or psoriatic arthritis and 219 healthy controls and individuals with joint pain without an underlying inflammatory cause. Diagnosis explained about 2% of gut taxonomic variability, which is comparable in magnitude to inflammatory bowel disease. We identified several candidate microbes with differential carriage patterns in patients with elevated blood markers for inflammation. Our results confirm and extend previous findings of increased carriage of typically oral and inflammatory taxa and decreased abundance and prevalence of typical gut clades, indicating that distal inflammatory conditions, as well as local conditions, correspond to alterations to the gut microbial composition. We identified several differentially encoded pathways in the gut microbiome of patients with inflammatory arthritis, including changes in vitamin B salvage and biosynthesis and enrichment of iron sequestration. Although several of these changes characteristic of inflammation could have causal roles, we hypothesize that they are mainly positive feedback responses to changes in host physiology and immune homeostasis. By connecting taxonomic alternations to functional alterations, this work expands our understanding of the shifts in the gut ecosystem that occur in response to systemic inflammation during arthritis.</p>
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spelling oxford-uuid:4bcc7d5e-b653-4c26-9ecc-e330d69775632023-08-11T11:05:06ZAlterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypesJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:4bcc7d5e-b653-4c26-9ecc-e330d6977563EnglishSymplectic ElementsAmerican Association for the Advancement of Science2023Thompson, KNBonham, KSIlott, NEColmenero, PBullers, SJBrough, IPearson, CMoussa, CKumar, VLam, LHJackson, MAKiriakidis, STaylor, PCMarsden, BBowness, PPowrie, FInflammatory Arthritis Microbiome Consortium (IAMC) investigators group<p>Musculoskeletal diseases affect up to 20% of adults worldwide. The gut microbiome has been implicated in inflammatory conditions, but large-scale metagenomic evaluations have not yet traced the routes by which immunity in the gut affects inflammatory arthritis. To characterize the community structure and associated functional processes driving gut microbial involvement in arthritis, the Inflammatory Arthritis Microbiome Consortium investigated 440 stool shotgun metagenomes comprising 221 adults diagnosed with rheumatoid arthritis, ankylosing spondylitis, or psoriatic arthritis and 219 healthy controls and individuals with joint pain without an underlying inflammatory cause. Diagnosis explained about 2% of gut taxonomic variability, which is comparable in magnitude to inflammatory bowel disease. We identified several candidate microbes with differential carriage patterns in patients with elevated blood markers for inflammation. Our results confirm and extend previous findings of increased carriage of typically oral and inflammatory taxa and decreased abundance and prevalence of typical gut clades, indicating that distal inflammatory conditions, as well as local conditions, correspond to alterations to the gut microbial composition. We identified several differentially encoded pathways in the gut microbiome of patients with inflammatory arthritis, including changes in vitamin B salvage and biosynthesis and enrichment of iron sequestration. Although several of these changes characteristic of inflammation could have causal roles, we hypothesize that they are mainly positive feedback responses to changes in host physiology and immune homeostasis. By connecting taxonomic alternations to functional alterations, this work expands our understanding of the shifts in the gut ecosystem that occur in response to systemic inflammation during arthritis.</p>
spellingShingle Thompson, KN
Bonham, KS
Ilott, NE
Colmenero, P
Bullers, SJ
Brough, I
Pearson, C
Moussa, C
Kumar, V
Lam, LH
Jackson, MA
Kiriakidis, S
Taylor, PC
Marsden, B
Bowness, P
Powrie, F
Alterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypes
title Alterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypes
title_full Alterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypes
title_fullStr Alterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypes
title_full_unstemmed Alterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypes
title_short Alterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypes
title_sort alterations in the gut microbiome implicate key taxa and metabolic pathways across inflammatory arthritis phenotypes
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