Distinct intestinal microbial signatures linked to accelerated systemic and intestinal biological aging
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Study information
-
Quality control
- Retracted paper
- Contamination issues suspected
- Batch effect issues suspected
- Uncontrolled confounding suspected
- Results are suspect (various reasons)
- Tags applied
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
Authors
Singh S, Giron LB, Shaikh MW, Shankaran S, Engen PA, Bogin ZR, Bambi SA, Goldman AR, Azevedo JLLC, Orgaz L, de Pedro N, González P, Giera M, Verhoeven A, Sánchez-López E, Pandrea I, Kannan T, Tanes CE, Bittinger K, Landay AL, Corley MJ, Keshavarzian A, Abdel-Mohsen M
Journal
Microbiome
Year
2024
Keywords:
Aging clocks, Biological aging, Gut, HIV, Intestines, Metabolome, Microbiome
BACKGROUND: People living with HIV (PLWH), even when viral replication is controlled through antiretroviral therapy (ART), experience persistent inflammation. This inflammation is partly attributed to intestinal microbial dysbiosis and translocation, which may lead to non-AIDS-related aging-associated comorbidities. The extent to which living with HIV - influenced by the infection itself, ART usage, sexual orientation, or other associated factors - affects the biological age of the intestines is unclear. Furthermore, the role of microbial dysbiosis and translocation in the biological aging of PLWH remains to be elucidated. To investigate these uncertainties, we used a systems biology approach, analyzing colon and ileal biopsies, blood samples, and stool specimens from PLWH on ART and people living without HIV (PLWoH) as controls. RESULTS: PLWH exhibit accelerated biological aging in the colon, ileum, and blood, as measured by various epigenetic aging clocks, compared to PLWoH. Investigating the relationship between microbial translocation and biological aging, PLWH had decreased levels of tight junction proteins in the intestines, along with increased microbial translocation. This intestinal permeability correlated with faster biological aging and increased inflammation. When investigating the relationship between microbial dysbiosis and biological aging, the intestines of PLWH had higher abundance of specific pro-inflammatory bacteria, such as Catenibacterium and Prevotella. These bacteria correlated with accelerated biological aging. Conversely, the intestines of PLWH had lower abundance of bacteria known for producing the anti-inflammatory short-chain fatty acids, such as Subdoligranulum and Erysipelotrichaceae, and these bacteria were associated with slower biological aging. Correlation networks revealed significant links between specific microbial genera in the colon and ileum (but not in feces), increased aging, a rise in pro-inflammatory microbe-related metabolites (e.g., those in the tryptophan metabolism pathway), and a decrease in anti-inflammatory metabolites like hippuric acid. CONCLUSIONS: We identified specific microbial compositions and microbiota-related metabolic pathways that are intertwined with intestinal and systemic biological aging. This microbial signature of biological aging is likely reflecting various factors including the HIV infection itself, ART usage, sexual orientation, and other aspects associated with living with HIV. A deeper understanding of the mechanisms underlying these connections could offer potential strategies to mitigate accelerated aging and its associated health complications. Video Abstract.
Experiment 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Subjects
- Location of subjects
- United States of America
- 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
- Colon Hindgut,Large bowel,Posterior intestine,Colon,colon
- Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
- HIV infection [X]Human immunodeficiency virus disease,[X]Human immunodeficiency virus disease (disorder),[X]Unspecified human immunodeficiency virus [HIV] disease,[X]Unspecified human immunodeficiency virus [HIV] disease (disorder),HIV - Human immunodeficiency virus infection,HIV INFECT,HIV Infection,HIV infection,HIV Infections,HIV infectious disease,HTLV III INFECT,HTLV III Infections,HTLV III LAV INFECT,HTLV III LAV Infections,HTLV WIII INFECTIONS,HTLV WIII LAV INFECTIONS,HTLV-III Infection,HTLV-III Infections,HTLV-III-LAV Infection,HTLV-III-LAV Infections,HUMAN IMMUNO VIRUS DIS,human immunodeficiency virus,Human immunodeficiency virus [HIV] disease,HUMAN IMMUNOdeficiency VIRUS [HIV] INFECTION,Human immunodeficiency virus caused disease or disorder,Human immunodeficiency virus disease,Human immunodeficiency virus disease (disorder),Human immunodeficiency virus disease or disorder,Human immunodeficiency virus infection,Human immunodeficiency virus infection (disorder),Human immunodeficiency virus infection, NOS,Human immunodeficiency virus infectious disease,human immunodeficiency virus infectious disease,Infection, HIV,Infection, HTLV-III,Infection, HTLV-III-LAV,Infections, HIV,Infections, HTLV-III,Infections, HTLV-III-LAV,LYMPHOTROPIC VIRUS TYPE III INFECTIONS HUMAN T,T LYMPHOTROPIC VIRUS TYPE III INFECT HUMAN,T Lymphotropic Virus Type III Infections, Human,T-Lymphotropic Virus Type III Infections, Human,Unspecified human immunodeficiency virus [HIV] disease (disorder),hIV infection
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Controls/ People living without HIV (PLWOH)
- Group 1 name Corresponds to the case (exposed) group for case-control studies
- People living with HIV on Antiretroviral Therapy (PLWH on ART)
- Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
- People with HIV infection on Anti-Retroviral Therapy(ART)
- Group 0 sample size Number of subjects in the control (unexposed) group
- 23
- Group 1 sample size Number of subjects in the case (exposed) group
- 25
Lab analysis
- Sequencing type
- 16S
- 16S variable region One or more hypervariable region(s) of the bacterial 16S gene
- V1-V2
- 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).
- relative abundances
- Statistical test
- Linear Regression
- Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
- 0.05
- 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
- age, body mass index, ethnic group, sex
Alpha Diversity
- Shannon Estimator of species richness and species evenness: more weight on species richness
- decreased
- Richness Number of species
- decreased
- Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
- decreased
Signature 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Figure 4D
Description: Log-scale differences in bacterial abundance across colon (triangle), between PLWoH and PLWH on ART.
Abundance in Group 1: increased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Alloprevotella | ||
| Catenibacterium | ||
| Enterobacteriaceae | ||
| Prevotella sp. |
Revision editor(s): Imaspecial, Fiddyhamma
Signature 2
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Figure 4D
Description: Log-scale differences in bacterial abundance across colon (triangle), between PLWoH and PLWH on ART.
Abundance in Group 1: decreased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Alistipes | ||
| Bacteroidales | ||
| Bacteroides | ||
| Faecalibacterium | ||
| Subdoligranulum | ||
| uncultured Erysipelotrichaceae bacterium | ||
| Coprococcus sp. |
Revision editor(s): Imaspecial, Fiddyhamma
Experiment 2
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Ileum Distal intestine,Intestinum ileum,Lower intestine,Posterior intestine,Ileum,ileum
Lab analysis
Statistical Analysis
Alpha Diversity
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- unchanged
- Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
- unchanged
Signature 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Fig 4D
Description: Log-scale differences in bacterial abundance across ileum (square), between PLWoH and PLWH on ART.
Abundance in Group 1: increased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Alloprevotella | ||
| Catenibacterium | ||
| Prevotella sp. | ||
| Prevotella sp. 1-8 |
Revision editor(s): Imaspecial, Fiddyhamma
Signature 2
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Fig 4D
Description: Log-scale differences in bacterial abundance across ileum (square), between PLWOH and PLWH on ART
Abundance in Group 1: decreased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Alistipes | ||
| Bacteroides | ||
| Subdoligranulum | ||
| uncultured Erysipelotrichaceae bacterium | ||
| Coprococcus sp. | ||
| Peptostreptococcaceae | ||
| Romboutsia |
Revision editor(s): Imaspecial, Fiddyhamma
Experiment 3
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Differences from previous experiment shown
Subjects
- 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
Lab analysis
Statistical Analysis
Alpha Diversity
- Shannon Estimator of species richness and species evenness: more weight on species richness
- unchanged
- Richness Number of species
- unchanged
- Faith Phylogenetic diversity, takes into account phylogenetic distance of all taxa identified in a sample
- unchanged
Signature 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Fig 4D
Description: Log-scale differences in bacterial abundance across feces (circle) between PLWOH and PLWH on ART.
Abundance in Group 1: increased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Catenibacterium | ||
| Prevotella sp. | ||
| Alloprevotella | ||
| Lachnospiraceae |
Revision editor(s): Imaspecial, Fiddyhamma
Signature 2
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Fig 4D
Description: Log-scale differences in bacterial abundance across feces (circle) between PLWOH and PLWH on ART.
Abundance in Group 1: decreased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| uncultured Erysipelotrichaceae bacterium | ||
| Alistipes | ||
| Peptostreptococcaceae | ||
| Bacteroides | ||
| Ruminococcus gauvreauii |
Revision editor(s): Imaspecial, Fiddyhamma
Experiment 4
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Colon , Feces Hindgut,Large bowel,Posterior intestine,Colon,colon,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
- Aging ageing,AGING BIOL,Aging, Biological,BIOL AGING,Biological Aging,Senescence,Aging,aging
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Colon Tissue Sample
- Group 1 name Corresponds to the case (exposed) group for case-control studies
- Fecal Sample
- Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
- Fecal sample collected from participants
- Group 0 sample size Number of subjects in the control (unexposed) group
- Not specified
- Group 1 sample size Number of subjects in the case (exposed) group
- Not specified
Lab analysis
Statistical Analysis
Signature 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Fig 4C
Description: Differential bacterial abundance between tissue and fecal samples on a logarithmic scale. Comparisons include colon vs. feces (red).
Abundance in Group 1: increased abundance in Fecal Sample
Revision editor(s): Imaspecial, Fiddyhamma
Signature 2
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Fig 4C
Description: Differential bacterial abundance between tissue and fecal samples on a logarithmic scale. Comparisons include colon vs. feces (red).
Abundance in Group 1: decreased abundance in Fecal Sample
Revision editor(s): Imaspecial, Fiddyhamma
Experiment 5
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Ileum , Feces Distal intestine,Intestinum ileum,Lower intestine,Posterior intestine,Ileum,ileum,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
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Ileum Tissue Sample
Lab analysis
Statistical Analysis
Signature 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Fig 4C
Description: Differential bacterial abundance between tissue and fecal samples on a logarithmic scale. Comparisons include Ileum vs. feces (blue).
Abundance in Group 1: increased abundance in Fecal Sample
Revision editor(s): Imaspecial, Fiddyhamma
Signature 2
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Fig 4C
Description: Differential bacterial abundance between tissue and fecal samples on a logarithmic scale. Comparisons include Ileum vs. feces (blue).
Abundance in Group 1: decreased abundance in Fecal Sample
Revision editor(s): Imaspecial, Fiddyhamma
Experiment 6
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Differences from previous experiment shown
Subjects
- 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
- HIV infection [X]Human immunodeficiency virus disease,[X]Human immunodeficiency virus disease (disorder),[X]Unspecified human immunodeficiency virus [HIV] disease,[X]Unspecified human immunodeficiency virus [HIV] disease (disorder),HIV - Human immunodeficiency virus infection,HIV INFECT,HIV Infection,HIV infection,HIV Infections,HIV infectious disease,HTLV III INFECT,HTLV III Infections,HTLV III LAV INFECT,HTLV III LAV Infections,HTLV WIII INFECTIONS,HTLV WIII LAV INFECTIONS,HTLV-III Infection,HTLV-III Infections,HTLV-III-LAV Infection,HTLV-III-LAV Infections,HUMAN IMMUNO VIRUS DIS,human immunodeficiency virus,Human immunodeficiency virus [HIV] disease,HUMAN IMMUNOdeficiency VIRUS [HIV] INFECTION,Human immunodeficiency virus caused disease or disorder,Human immunodeficiency virus disease,Human immunodeficiency virus disease (disorder),Human immunodeficiency virus disease or disorder,Human immunodeficiency virus infection,Human immunodeficiency virus infection (disorder),Human immunodeficiency virus infection, NOS,Human immunodeficiency virus infectious disease,human immunodeficiency virus infectious disease,Infection, HIV,Infection, HTLV-III,Infection, HTLV-III-LAV,Infections, HIV,Infections, HTLV-III,Infections, HTLV-III-LAV,LYMPHOTROPIC VIRUS TYPE III INFECTIONS HUMAN T,T LYMPHOTROPIC VIRUS TYPE III INFECT HUMAN,T Lymphotropic Virus Type III Infections, Human,T-Lymphotropic Virus Type III Infections, Human,Unspecified human immunodeficiency virus [HIV] disease (disorder),hIV infection
- Group 0 name Corresponds to the control (unexposed) group for case-control studies
- Controls/ People living without HIV (PLWOH)
- Group 1 name Corresponds to the case (exposed) group for case-control studies
- People living with HIV on Antiretroviral Therapy (PLWH on ART)
- Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
- People with HIV infection on Anti-Retroviral Therapy(ART)
Lab analysis
Statistical Analysis
Alpha Diversity
- Richness Number of species
- decreased
Signature 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Additional figure 10E
Description: Estimated log difference between heterosexual PLWH on ART and heterosexual PLWoH
Abundance in Group 1: decreased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Ruminococcus sp. | ||
| unclassified Oscillospiraceae | ||
| Bacteroides |
Revision editor(s): Fiddyhamma
Experiment 7
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Ileum Distal intestine,Intestinum ileum,Lower intestine,Posterior intestine,Ileum,ileum
Lab analysis
Statistical Analysis
Alpha Diversity
- Richness Number of species
- decreased
Signature 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Additional figure 10E
Description: Estimated log difference between heterosexual PLWH on ART and heterosexual PLWoH
Abundance in Group 1: increased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Enterobacteriaceae |
Revision editor(s): Fiddyhamma
Signature 2
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Additional figure 10E
Description: Estimated log difference between heterosexual PLWH on ART and heterosexual PLWoH
Abundance in Group 1: decreased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Bacteroides | ||
| Coprococcus sp. | ||
| Ruminococcus sp. | ||
| Christensenellaceae R7Christensenellaceae R7 |
Revision editor(s): Fiddyhamma
Experiment 8
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Differences from previous experiment shown
Subjects
- Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
- Colon Hindgut,Large bowel,Posterior intestine,Colon,colon
Lab analysis
Statistical Analysis
Alpha Diversity
- Richness Number of species
- decreased
Signature 1
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Additional figure 10E
Description: Estimated log difference between heterosexual PLWH on ART and heterosexual PLWoH
Abundance in Group 1: increased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Enterobacteriaceae |
Revision editor(s): Fiddyhamma
Signature 2
Reviewed Marked as Reviewed by Svetlana up on 2024-11-14
Source: Additional figure 10E
Description: Estimated log difference between heterosexual PLWH on ART and heterosexual PLWoH
Abundance in Group 1: decreased abundance in People living with HIV on Antiretroviral Therapy (PLWH on ART)
| NCBI | Quality Control | Links |
|---|---|---|
| Bacteroides | ||
| Coprococcus sp. | ||
| Ruminococcus sp. | ||
| Christensenellaceae R7Christensenellaceae R7 |
Revision editor(s): Fiddyhamma
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