Depression in Individuals Coinfected with HIV and HCV Is Associated with Systematic Differences in the Gut Microbiome and Metabolome

ABSTRACT Depression is influenced by the structure, diversity, and composition of the gut microbiome. Although depression has been described previously in human immunodeficiency virus (HIV) and hepatitis C virus (HCV) monoinfections, and to a lesser extent in HIV-HCV coinfection, research on the int...

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Autores principales: Bryn C. Taylor, Kelly C. Weldon, Ronald J. Ellis, Donald Franklin, Tobin Groth, Emily C. Gentry, Anupriya Tripathi, Daniel McDonald, Gregory Humphrey, MacKenzie Bryant, Julia Toronczak, Tara Schwartz, Michelli F. Oliveira, Robert Heaton, Igor Grant, Sara Gianella, Scott Letendre, Austin Swafford, Pieter C. Dorrestein, Rob Knight
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:4d000583e1cf4e279932e95eba1e01762021-12-02T19:46:19ZDepression in Individuals Coinfected with HIV and HCV Is Associated with Systematic Differences in the Gut Microbiome and Metabolome10.1128/mSystems.00465-202379-5077https://doaj.org/article/4d000583e1cf4e279932e95eba1e01762020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00465-20https://doaj.org/toc/2379-5077ABSTRACT Depression is influenced by the structure, diversity, and composition of the gut microbiome. Although depression has been described previously in human immunodeficiency virus (HIV) and hepatitis C virus (HCV) monoinfections, and to a lesser extent in HIV-HCV coinfection, research on the interplay between depression and the gut microbiome in these disease states is limited. Here, we characterized the gut microbiome using 16S rRNA amplicon sequencing of fecal samples from 373 participants who underwent a comprehensive neuropsychiatric assessment and the gut metabolome on a subset of these participants using untargeted metabolomics with liquid chromatography-mass spectrometry. We observed that the gut microbiome and metabolome were distinct between HIV-positive and -negative individuals. HCV infection had a large association with the microbiome that was not confounded by drug use. Therefore, we classified the participants by HIV and HCV infection status (HIV-monoinfected, HIV-HCV coinfected, or uninfected). The three groups significantly differed in their gut microbiome (unweighted UniFrac distances) and metabolome (Bray-Curtis distances). Coinfected individuals also had lower alpha diversity. Within each of the three groups, we evaluated lifetime major depressive disorder (MDD) and current Beck Depression Inventory-II. We found that the gut microbiome differed between depression states only in coinfected individuals. Coinfected individuals with a lifetime history of MDD were enriched in primary and secondary bile acids, as well as taxa previously identified in people with MDD. Collectively, we observe persistent signatures associated with depression only in coinfected individuals, suggesting that HCV itself, or interactions between HCV and HIV, may drive HIV-related neuropsychiatric differences. IMPORTANCE The human gut microbiome influences depression. Differences between the microbiomes of HIV-infected and uninfected individuals have been described, but it is not known whether these are due to HIV itself, or to common HIV comorbidities such as HCV coinfection. Limited research has explored the influence of the microbiome on depression within these groups. Here, we characterized the microbial community and metabolome in the stools from 373 people, noting the presence of current or lifetime depression as well as their HIV and HCV infection status. Our findings provide additional evidence that individuals with HIV have different microbiomes which are further altered by HCV coinfection. In individuals coinfected with both HIV and HCV, we identified microbes and molecules that were associated with depression. These results suggest that the interplay of HIV and HCV and the gut microbiome may contribute to the HIV-associated neuropsychiatric problems.Bryn C. TaylorKelly C. WeldonRonald J. EllisDonald FranklinTobin GrothEmily C. GentryAnupriya TripathiDaniel McDonaldGregory HumphreyMacKenzie BryantJulia ToronczakTara SchwartzMichelli F. OliveiraRobert HeatonIgor GrantSara GianellaScott LetendreAustin SwaffordPieter C. DorresteinRob KnightAmerican Society for MicrobiologyarticleHIVhepatitis Cmicrobiomedepressiongut microbiomehepatitis C virusMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution DOAJ
collection DOAJ
language EN
topic HIV
hepatitis C
microbiome
depression
gut microbiome
hepatitis C virus
Microbiology
QR1-502
spellingShingle HIV
hepatitis C
microbiome
depression
gut microbiome
hepatitis C virus
Microbiology
QR1-502
Bryn C. Taylor
Kelly C. Weldon
Ronald J. Ellis
Donald Franklin
Tobin Groth
Emily C. Gentry
Anupriya Tripathi
Daniel McDonald
Gregory Humphrey
MacKenzie Bryant
Julia Toronczak
Tara Schwartz
Michelli F. Oliveira
Robert Heaton
Igor Grant
Sara Gianella
Scott Letendre
Austin Swafford
Pieter C. Dorrestein
Rob Knight
Depression in Individuals Coinfected with HIV and HCV Is Associated with Systematic Differences in the Gut Microbiome and Metabolome
description ABSTRACT Depression is influenced by the structure, diversity, and composition of the gut microbiome. Although depression has been described previously in human immunodeficiency virus (HIV) and hepatitis C virus (HCV) monoinfections, and to a lesser extent in HIV-HCV coinfection, research on the interplay between depression and the gut microbiome in these disease states is limited. Here, we characterized the gut microbiome using 16S rRNA amplicon sequencing of fecal samples from 373 participants who underwent a comprehensive neuropsychiatric assessment and the gut metabolome on a subset of these participants using untargeted metabolomics with liquid chromatography-mass spectrometry. We observed that the gut microbiome and metabolome were distinct between HIV-positive and -negative individuals. HCV infection had a large association with the microbiome that was not confounded by drug use. Therefore, we classified the participants by HIV and HCV infection status (HIV-monoinfected, HIV-HCV coinfected, or uninfected). The three groups significantly differed in their gut microbiome (unweighted UniFrac distances) and metabolome (Bray-Curtis distances). Coinfected individuals also had lower alpha diversity. Within each of the three groups, we evaluated lifetime major depressive disorder (MDD) and current Beck Depression Inventory-II. We found that the gut microbiome differed between depression states only in coinfected individuals. Coinfected individuals with a lifetime history of MDD were enriched in primary and secondary bile acids, as well as taxa previously identified in people with MDD. Collectively, we observe persistent signatures associated with depression only in coinfected individuals, suggesting that HCV itself, or interactions between HCV and HIV, may drive HIV-related neuropsychiatric differences. IMPORTANCE The human gut microbiome influences depression. Differences between the microbiomes of HIV-infected and uninfected individuals have been described, but it is not known whether these are due to HIV itself, or to common HIV comorbidities such as HCV coinfection. Limited research has explored the influence of the microbiome on depression within these groups. Here, we characterized the microbial community and metabolome in the stools from 373 people, noting the presence of current or lifetime depression as well as their HIV and HCV infection status. Our findings provide additional evidence that individuals with HIV have different microbiomes which are further altered by HCV coinfection. In individuals coinfected with both HIV and HCV, we identified microbes and molecules that were associated with depression. These results suggest that the interplay of HIV and HCV and the gut microbiome may contribute to the HIV-associated neuropsychiatric problems.
format article
author Bryn C. Taylor
Kelly C. Weldon
Ronald J. Ellis
Donald Franklin
Tobin Groth
Emily C. Gentry
Anupriya Tripathi
Daniel McDonald
Gregory Humphrey
MacKenzie Bryant
Julia Toronczak
Tara Schwartz
Michelli F. Oliveira
Robert Heaton
Igor Grant
Sara Gianella
Scott Letendre
Austin Swafford
Pieter C. Dorrestein
Rob Knight
author_facet Bryn C. Taylor
Kelly C. Weldon
Ronald J. Ellis
Donald Franklin
Tobin Groth
Emily C. Gentry
Anupriya Tripathi
Daniel McDonald
Gregory Humphrey
MacKenzie Bryant
Julia Toronczak
Tara Schwartz
Michelli F. Oliveira
Robert Heaton
Igor Grant
Sara Gianella
Scott Letendre
Austin Swafford
Pieter C. Dorrestein
Rob Knight
author_sort Bryn C. Taylor
title Depression in Individuals Coinfected with HIV and HCV Is Associated with Systematic Differences in the Gut Microbiome and Metabolome
title_short Depression in Individuals Coinfected with HIV and HCV Is Associated with Systematic Differences in the Gut Microbiome and Metabolome
title_full Depression in Individuals Coinfected with HIV and HCV Is Associated with Systematic Differences in the Gut Microbiome and Metabolome
title_fullStr Depression in Individuals Coinfected with HIV and HCV Is Associated with Systematic Differences in the Gut Microbiome and Metabolome
title_full_unstemmed Depression in Individuals Coinfected with HIV and HCV Is Associated with Systematic Differences in the Gut Microbiome and Metabolome
title_sort depression in individuals coinfected with hiv and hcv is associated with systematic differences in the gut microbiome and metabolome
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/4d000583e1cf4e279932e95eba1e0176
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