Gut dysbiosis narrative in psoriasis: matched-pair approach identifies only subtle shifts correlated with elevated fecal calprotectin

ABSTRACT Many studies have reported gut microbiome alterations in psoriasis patients, suggesting dysbiosis. While evidence for dysbiosis and its link to pathogenesis remains inconclusive, murine models of psoriasis suggest that gut microbiome alterations develop in response to psoriasis-like inflamm...

Full description

Saved in:
Bibliographic Details
Main Authors: Bayazit Yunusbayev, Anna Bogdanova, Nadezhda Nadyrchenko, Lavrentii Danilov, Viktor Bogdanov, Grigory Sergeev, Radick Altinbaev, Fanil Bilalov, Milyausha Yunusbaeva
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.01382-24
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1841556089642942464
author Bayazit Yunusbayev
Anna Bogdanova
Nadezhda Nadyrchenko
Lavrentii Danilov
Viktor Bogdanov
Grigory Sergeev
Radick Altinbaev
Fanil Bilalov
Milyausha Yunusbaeva
author_facet Bayazit Yunusbayev
Anna Bogdanova
Nadezhda Nadyrchenko
Lavrentii Danilov
Viktor Bogdanov
Grigory Sergeev
Radick Altinbaev
Fanil Bilalov
Milyausha Yunusbaeva
author_sort Bayazit Yunusbayev
collection DOAJ
description ABSTRACT Many studies have reported gut microbiome alterations in psoriasis patients, suggesting dysbiosis. While evidence for dysbiosis and its link to pathogenesis remains inconclusive, murine models of psoriasis suggest that gut microbiome alterations develop in response to psoriasis-like inflammation. Hence, the dominant narrative about gut microbiome alterations’ impact on disease should be evaluated critically with more data and a well-powered approach. In this case-control study, we used deep sequencing of fecal samples from 53 psoriasis patients and 47 healthy donors to reconstruct the strain/species-level content of the gut microbiome. Unlike previous studies, we first identified matched pairs for each patient with healthy donors to adjust for microbiome variability and increase power. We found no evidence for depleted gut community diversity and apparent divergence in structure between patients and healthy individuals. However, our matched-pair approach identified a subtle but systematic increase in select bacteria among patients, e.g., Megasphaera elsdenii and Eubacterium CAG 180. We next showed that these enriched species were correlated with elevated biomarkers of intestinal and systemic inflammation and liver function. Functionally, one of the top species, Megasphaera elsdenii, is a potent lactate utilizer in the context of intestinal lactic acidosis and inflammation. While our findings hardly support overt dysbiosis in the large intestine, the observed microbial changes correlate with moderately elevated calprotectin, albeit at levels not enough to diagnose ongoing inflammation. Hence, the sources of elevated inflammatory markers in patients’ intestines remain unclear and warrant further investigation to clarify their cause-and-effect relationship with the disease.IMPORTANCEWith sufficient taxonomic resolution and sample size, this study critically evaluates new and published data on the gut microbiome in psoriasis patients. It shows that observed taxonomic changes in patients are modest and do not meet strict criteria for gut dysbiosis, at least in the large intestine. Instead, observed taxonomic changes in psoriasis patients can be explained by the microbial response to possible low-grade inflammation with unknown localization in the intestine and unclear impact on the host. The authors point out that published endoscopic data point to the small intestine as the site of gut inflammation. Therefore, further research focused on the small intestine would be informative to clarify the hypothetical gut-psoriasis link.
format Article
id doaj-art-5c40f01de6064584842fd2079b94686b
institution Kabale University
issn 2165-0497
language English
publishDate 2025-01-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj-art-5c40f01de6064584842fd2079b94686b2025-01-07T14:05:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-01-0113110.1128/spectrum.01382-24Gut dysbiosis narrative in psoriasis: matched-pair approach identifies only subtle shifts correlated with elevated fecal calprotectinBayazit Yunusbayev0Anna Bogdanova1Nadezhda Nadyrchenko2Lavrentii Danilov3Viktor Bogdanov4Grigory Sergeev5Radick Altinbaev6Fanil Bilalov7Milyausha Yunusbaeva8Institute of Translational Biomedicine, Saint-Petersburg State University, Saint-Petersburg, RussiaSCAMT institute, ITMO University, Saint Petersburg, RussiaRepublican Dermatovenerologic Dispensary, Ufa, RussiaDepartment of Genetics and Biotechnology, Saint-Petersburg State University, Saint-Petersburg, RussiaMultiomics Laboratory, Moscow Institute of Physics and Technology, Moscow, RussiaSCAMT institute, ITMO University, Saint Petersburg, RussiaInstitute of Higher Nervous Activity and Neurophysiology of RAS, Moscow, RussiaDepartment of Laboratory Medicine, Bashkir State Medical University, Ufa, RussiaInstitute of Translational Biomedicine, Saint-Petersburg State University, Saint-Petersburg, RussiaABSTRACT Many studies have reported gut microbiome alterations in psoriasis patients, suggesting dysbiosis. While evidence for dysbiosis and its link to pathogenesis remains inconclusive, murine models of psoriasis suggest that gut microbiome alterations develop in response to psoriasis-like inflammation. Hence, the dominant narrative about gut microbiome alterations’ impact on disease should be evaluated critically with more data and a well-powered approach. In this case-control study, we used deep sequencing of fecal samples from 53 psoriasis patients and 47 healthy donors to reconstruct the strain/species-level content of the gut microbiome. Unlike previous studies, we first identified matched pairs for each patient with healthy donors to adjust for microbiome variability and increase power. We found no evidence for depleted gut community diversity and apparent divergence in structure between patients and healthy individuals. However, our matched-pair approach identified a subtle but systematic increase in select bacteria among patients, e.g., Megasphaera elsdenii and Eubacterium CAG 180. We next showed that these enriched species were correlated with elevated biomarkers of intestinal and systemic inflammation and liver function. Functionally, one of the top species, Megasphaera elsdenii, is a potent lactate utilizer in the context of intestinal lactic acidosis and inflammation. While our findings hardly support overt dysbiosis in the large intestine, the observed microbial changes correlate with moderately elevated calprotectin, albeit at levels not enough to diagnose ongoing inflammation. Hence, the sources of elevated inflammatory markers in patients’ intestines remain unclear and warrant further investigation to clarify their cause-and-effect relationship with the disease.IMPORTANCEWith sufficient taxonomic resolution and sample size, this study critically evaluates new and published data on the gut microbiome in psoriasis patients. It shows that observed taxonomic changes in patients are modest and do not meet strict criteria for gut dysbiosis, at least in the large intestine. Instead, observed taxonomic changes in psoriasis patients can be explained by the microbial response to possible low-grade inflammation with unknown localization in the intestine and unclear impact on the host. The authors point out that published endoscopic data point to the small intestine as the site of gut inflammation. Therefore, further research focused on the small intestine would be informative to clarify the hypothetical gut-psoriasis link.https://journals.asm.org/doi/10.1128/spectrum.01382-24gut microbiotadysbiosislow-grade Inflammationpsoriasislactate
spellingShingle Bayazit Yunusbayev
Anna Bogdanova
Nadezhda Nadyrchenko
Lavrentii Danilov
Viktor Bogdanov
Grigory Sergeev
Radick Altinbaev
Fanil Bilalov
Milyausha Yunusbaeva
Gut dysbiosis narrative in psoriasis: matched-pair approach identifies only subtle shifts correlated with elevated fecal calprotectin
Microbiology Spectrum
gut microbiota
dysbiosis
low-grade Inflammation
psoriasis
lactate
title Gut dysbiosis narrative in psoriasis: matched-pair approach identifies only subtle shifts correlated with elevated fecal calprotectin
title_full Gut dysbiosis narrative in psoriasis: matched-pair approach identifies only subtle shifts correlated with elevated fecal calprotectin
title_fullStr Gut dysbiosis narrative in psoriasis: matched-pair approach identifies only subtle shifts correlated with elevated fecal calprotectin
title_full_unstemmed Gut dysbiosis narrative in psoriasis: matched-pair approach identifies only subtle shifts correlated with elevated fecal calprotectin
title_short Gut dysbiosis narrative in psoriasis: matched-pair approach identifies only subtle shifts correlated with elevated fecal calprotectin
title_sort gut dysbiosis narrative in psoriasis matched pair approach identifies only subtle shifts correlated with elevated fecal calprotectin
topic gut microbiota
dysbiosis
low-grade Inflammation
psoriasis
lactate
url https://journals.asm.org/doi/10.1128/spectrum.01382-24
work_keys_str_mv AT bayazityunusbayev gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin
AT annabogdanova gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin
AT nadezhdanadyrchenko gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin
AT lavrentiidanilov gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin
AT viktorbogdanov gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin
AT grigorysergeev gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin
AT radickaltinbaev gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin
AT fanilbilalov gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin
AT milyaushayunusbaeva gutdysbiosisnarrativeinpsoriasismatchedpairapproachidentifiesonlysubtleshiftscorrelatedwithelevatedfecalcalprotectin