Differences in the gut microbiome across typical ageing and in Parkinson's disease

From BugSigDB
Reviewed Marked as Reviewed by Svetlana up on 2025-3-4
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Nuzum ND, Szymlek-Gay EA, Loke S, Dawson SL, Teo WP, Hendy AM, Loughman A, Macpherson H
Journal
Neuropharmacology
Year
2023
Keywords:
Aging, Gut-brain-axis, Microbiome, Microbiota, PD, Short chain fatty acids
The microbiota-gut-brain axis' role in Parkinson's disease (PD) pathophysiology, and how this differs from typical ageing, is poorly understood. Presently, gut-bacterial diversity, taxonomic abundance and metabolic bacterial pathways were compared across healthy young (n = 22, 18-35 years), healthy older (n = 33, 50-80 years), and PD groups (n = 18, 50-80 years) using shotgun sequencing and compositional data analysis. Associations between the gut-microbiome and PD symptoms, and between lifestyle factors (fibre intake, physical activity, and sleep) and the gut-microbiome were conducted. Alpha-diversity did not differ between PD participants and older adults, whilst beta-diversity differed between these groups. Lower abundance of Butyricimonas synergistica, a butyrate-producer, was associated with worse PD non-motor symptoms in the PD group. Regarding typical ageing, Bifidobacterium bifidum, was greater in the younger compared to older group, with no difference between the older and PD group. Abundance of metabolic pathways related to butyrate production did not differ among the groups, while other metabolic pathways differed among the three groups. Sleep efficiency was positively associated with Roseburia inulinivorans in the older group. These results highlight the relevance of gut-microbiota to PD and that reduced butyrate-production may be involved with PD pathophysiology. Future studies should account for lifestyle factors when investigating gut-microbiomes across ageing and in PD. This article is part of the Special Issue on "Microbiome & the Brain: Mechanisms & Maladies".

Experiment 1


Reviewed Marked as Reviewed by Svetlana up on 2025-3-4

Curated date: 2025/02/28

Curator: KateRasheed

Revision editor(s): KateRasheed

Subjects

Location of subjects
Australia
Host species Species from which microbiome was sampled. Contact us to have more species added.
Homo sapiens
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Parkinson's disease IDIOPATHIC PARKINSON DIS,Idiopathic Parkinson Disease,Idiopathic Parkinson's Disease,IDIOPATHIC PARKINSONS DIS,Idiopathic PD,LEWY BODY PARKINSON DIS,Lewy Body Parkinson Disease,Lewy Body Parkinson's Disease,Paralysis agitans,paralysis agitans,PARKINSON DIS,PARKINSON DIS IDIOPATHIC,Parkinson disease,Parkinson Disease, Idiopathic,Parkinson syndrome,Parkinson's,Parkinson's disease,Parkinson's disease (disorder),Parkinson's disease NOS,Parkinson's disease NOS (disorder),Parkinson's Disease, Idiopathic,Parkinson's Disease, Lewy Body,Parkinson's syndrome,Parkinsonian disorder,Parkinsonism, Primary,Parkinsons,PARKINSONS DIS,PARKINSONS DIS IDIOPATHIC,PARKINSONS DIS LEWY BODY,Parkinsons disease,Primary Parkinsonism,parkinson's disease
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Healthy younger (HY)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Healthy older (HO)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Healthy older (HO) refers to patients who are 50-80 years and had no neurological or neurodegenerative conditions, no first-degree relatives with PD, scores of ≥24/30 on the Montreal Cognitive assessment (MoCA) or ≥ 17/22 for the MoCA-Blind (remote assessment).
Group 0 sample size Number of subjects in the control (unexposed) group
22
Group 1 sample size Number of subjects in the case (exposed) group
33
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
3 months

Lab analysis

Sequencing type
WMS
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
Not specified
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
centered log-ratio
Statistical test
MaAsLin2
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.1
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
Yes
Matched on Factors on which subjects have been matched on in a case-control study
sex

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged
Inverse Simpson Modification of Simpsons index D as 1/D to obtain high values in datasets of high diversity and vice versa
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2025-3-4

Curated date: 2025/02/28

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Fig. 2, Fig. S1B

Description: Significantly differential abundance of taxa between healthy young and healthy older groups

Abundance in Group 1: decreased abundance in Healthy older (HO)

NCBI Quality ControlLinks
Bifidobacterium bifidum

Revision editor(s): KateRasheed

Experiment 2


Reviewed Marked as Reviewed by Svetlana up on 2025-3-4

Curated date: 2025/02/28

Curator: KateRasheed

Revision editor(s): KateRasheed

Differences from previous experiment shown

Subjects

Lab analysis

Statistical Analysis

Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
body mass index, sex, Confounders controlled for: "gastrointestinal symptoms" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.gastrointestinal symptoms, Confounders controlled for: "number of medications" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.number of medications, Confounders controlled for: "dietary fibre intake" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.dietary fibre intake

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged
Inverse Simpson Modification of Simpsons index D as 1/D to obtain high values in datasets of high diversity and vice versa
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2025-3-4

Curated date: 2025/02/28

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Fig. 2, Fig. S1B

Description: Significantly differential abundance of taxa between healthy young and healthy older groups after adjusting for covariates.

Abundance in Group 1: decreased abundance in Healthy older (HO)

NCBI Quality ControlLinks
Bifidobacterium bifidum

Revision editor(s): KateRasheed

Experiment 3


Reviewed Marked as Reviewed by Svetlana up on 2025-3-4

Curated date: 2025/02/28

Curator: KateRasheed

Revision editor(s): KateRasheed

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
Healthy older (HO)
Group 1 name Corresponds to the case (exposed) group for case-control studies
Parkinson’s disease patients (PD)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
PD refers to patients who are 50–80 years; having PD diagnosis which was determined through an independent neurologist. These individuals had to have mild-moderate PD as assessed via the Movement Disorder Society Unified Parkinson’s Disease Rating Scale stage-II form (MDS-UPDRS-II); which covers the motor experiences of daily living, no cases of early-onset PD i.e., diagnosis after 50 years of age, and MoCA scores for the PD group were set at ≥ 21/30 and ≥ 15/22 for the standard and MoCA-Blind respectively.
Group 0 sample size Number of subjects in the control (unexposed) group
33
Group 1 sample size Number of subjects in the case (exposed) group
18

Lab analysis

Statistical Analysis

Matched on Factors on which subjects have been matched on in a case-control study
age, sex
Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
Not specified

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged
Inverse Simpson Modification of Simpsons index D as 1/D to obtain high values in datasets of high diversity and vice versa
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2025-3-4

Curated date: 2025/02/28

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Fig. S1A

Description: Significantly differential abundance of taxa between PD and healthy older groups.

Abundance in Group 1: increased abundance in Parkinson’s disease patients (PD)

NCBI Quality ControlLinks
Pseudomonadota

Revision editor(s): KateRasheed

Experiment 4


Reviewed Marked as Reviewed by Svetlana up on 2025-3-4

Curated date: 2025/02/28

Curator: KateRasheed

Revision editor(s): KateRasheed

Differences from previous experiment shown

Subjects

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
PD refers to patients who are 50–80 years; having PD diagnosis which was determined through an independent neurologist. These individuals had to have mild-moderate PD as assessed via the Movement Disorder Society Unified Parkinson’s Disease Rating Scale stage-II form (MDS-UPDRS-II); which covers the motor experiences of daily living, no cases of early-onset PD i.e., diagnosis after 50 years of age, and MoCA scores for the PD group were set at ≥ 21/30 and ≥ 15/22 for the standard and MoCA-Blind respectively.

Lab analysis

Statistical Analysis

Confounders controlled for Confounding factors that have been accounted for by stratification or model adjustment
body mass index, sex, Confounders controlled for: "gastrointestinal symptoms" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.gastrointestinal symptoms, Confounders controlled for: "number of medications" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.number of medications, Confounders controlled for: "dietary fibre intake" is not in the list (abnormal glucose tolerance, acetaldehyde, acute graft vs. host disease, acute lymphoblastic leukemia, acute myeloid leukemia, adenoma, age, AIDS, alcohol consumption measurement, alcohol drinking, ...) of allowed values.dietary fibre intake

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Simpson Estimator of species richness and species evenness: more weight on species evenness
unchanged
Inverse Simpson Modification of Simpsons index D as 1/D to obtain high values in datasets of high diversity and vice versa
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2025-3-4

Curated date: 2025/02/28

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: In text of the "Phylum level" section

Description: Significantly differential abundance of taxa between PD and healthy older groups after adjusting for covariates.

Abundance in Group 1: increased abundance in Parkinson’s disease patients (PD)

NCBI Quality ControlLinks
Pseudomonadota

Revision editor(s): KateRasheed