Respiratory Viral Infection Alters the Gut Microbiota by Inducing Inappetence

ABSTRACT Respiratory viral infections are extremely common, but their impacts on the composition and function of the gut microbiota are poorly understood. We previously observed a significant change in the gut microbiota after viral lung infection. Here, we show that weight loss during respiratory s...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Helen T. Groves, Sophie L. Higham, Miriam F. Moffatt, Michael J. Cox, John S. Tregoning
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://doaj.org/article/5e5b8288553e42c09ce4d34ce2f4933c
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:5e5b8288553e42c09ce4d34ce2f4933c
record_format dspace
spelling oai:doaj.org-article:5e5b8288553e42c09ce4d34ce2f4933c2021-11-15T15:56:58ZRespiratory Viral Infection Alters the Gut Microbiota by Inducing Inappetence10.1128/mBio.03236-192150-7511https://doaj.org/article/5e5b8288553e42c09ce4d34ce2f4933c2020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03236-19https://doaj.org/toc/2150-7511ABSTRACT Respiratory viral infections are extremely common, but their impacts on the composition and function of the gut microbiota are poorly understood. We previously observed a significant change in the gut microbiota after viral lung infection. Here, we show that weight loss during respiratory syncytial virus (RSV) or influenza virus infection was due to decreased food consumption, and that the fasting of mice altered gut microbiota composition independently of infection. While the acute phase tumor necrosis factor alpha (TNF-α) response drove early weight loss and inappetence during RSV infection, this was not sufficient to induce changes in the gut microbiota. However, the depletion of CD8+ cells increased food intake and prevented weight loss, resulting in a reversal of the gut microbiota changes normally observed during RSV infection. Viral infection also led to changes in the fecal gut metabolome, with a significant shift in lipid metabolism. Sphingolipids, polyunsaturated fatty acids (PUFAs), and the short-chain fatty acid (SCFA) valerate were all increased in abundance in the fecal metabolome following RSV infection. Whether this and the impact of infection-induced anorexia on the gut microbiota are part of a protective anti-inflammatory response during respiratory viral infections remains to be determined. IMPORTANCE The gut microbiota has an important role in health and disease: gut bacteria can generate metabolites that alter the function of immune cells systemically. Understanding the factors that can lead to changes in the gut microbiome may help to inform therapeutic interventions. This is the first study to systematically dissect the pathway of events from viral lung infection to changes in gut microbiota. We show that the cellular immune response to viral lung infection induces inappetence, which in turn alters the gut microbiome and metabolome. Strikingly, there was an increase in lipids that have been associated with the resolution of disease. This opens up new paths of investigation: first, what is the (presumably secreted) factor made by the T cells that can induce inappetence? Second, is inappetence an adaptation that accelerates recovery from infection, and if so, does the microbiome play a role in this?Helen T. GrovesSophie L. HighamMiriam F. MoffattMichael J. CoxJohn S. TregoningAmerican Society for MicrobiologyarticleappetitemetabolomemicrobiomeT celllung infectionrespiratory syncytial virusMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution DOAJ
collection DOAJ
language EN
topic appetite
metabolome
microbiome
T cell
lung infection
respiratory syncytial virus
Microbiology
QR1-502
spellingShingle appetite
metabolome
microbiome
T cell
lung infection
respiratory syncytial virus
Microbiology
QR1-502
Helen T. Groves
Sophie L. Higham
Miriam F. Moffatt
Michael J. Cox
John S. Tregoning
Respiratory Viral Infection Alters the Gut Microbiota by Inducing Inappetence
description ABSTRACT Respiratory viral infections are extremely common, but their impacts on the composition and function of the gut microbiota are poorly understood. We previously observed a significant change in the gut microbiota after viral lung infection. Here, we show that weight loss during respiratory syncytial virus (RSV) or influenza virus infection was due to decreased food consumption, and that the fasting of mice altered gut microbiota composition independently of infection. While the acute phase tumor necrosis factor alpha (TNF-α) response drove early weight loss and inappetence during RSV infection, this was not sufficient to induce changes in the gut microbiota. However, the depletion of CD8+ cells increased food intake and prevented weight loss, resulting in a reversal of the gut microbiota changes normally observed during RSV infection. Viral infection also led to changes in the fecal gut metabolome, with a significant shift in lipid metabolism. Sphingolipids, polyunsaturated fatty acids (PUFAs), and the short-chain fatty acid (SCFA) valerate were all increased in abundance in the fecal metabolome following RSV infection. Whether this and the impact of infection-induced anorexia on the gut microbiota are part of a protective anti-inflammatory response during respiratory viral infections remains to be determined. IMPORTANCE The gut microbiota has an important role in health and disease: gut bacteria can generate metabolites that alter the function of immune cells systemically. Understanding the factors that can lead to changes in the gut microbiome may help to inform therapeutic interventions. This is the first study to systematically dissect the pathway of events from viral lung infection to changes in gut microbiota. We show that the cellular immune response to viral lung infection induces inappetence, which in turn alters the gut microbiome and metabolome. Strikingly, there was an increase in lipids that have been associated with the resolution of disease. This opens up new paths of investigation: first, what is the (presumably secreted) factor made by the T cells that can induce inappetence? Second, is inappetence an adaptation that accelerates recovery from infection, and if so, does the microbiome play a role in this?
format article
author Helen T. Groves
Sophie L. Higham
Miriam F. Moffatt
Michael J. Cox
John S. Tregoning
author_facet Helen T. Groves
Sophie L. Higham
Miriam F. Moffatt
Michael J. Cox
John S. Tregoning
author_sort Helen T. Groves
title Respiratory Viral Infection Alters the Gut Microbiota by Inducing Inappetence
title_short Respiratory Viral Infection Alters the Gut Microbiota by Inducing Inappetence
title_full Respiratory Viral Infection Alters the Gut Microbiota by Inducing Inappetence
title_fullStr Respiratory Viral Infection Alters the Gut Microbiota by Inducing Inappetence
title_full_unstemmed Respiratory Viral Infection Alters the Gut Microbiota by Inducing Inappetence
title_sort respiratory viral infection alters the gut microbiota by inducing inappetence
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/5e5b8288553e42c09ce4d34ce2f4933c
work_keys_str_mv AT helentgroves respiratoryviralinfectionaltersthegutmicrobiotabyinducinginappetence
AT sophielhigham respiratoryviralinfectionaltersthegutmicrobiotabyinducinginappetence
AT miriamfmoffatt respiratoryviralinfectionaltersthegutmicrobiotabyinducinginappetence
AT michaeljcox respiratoryviralinfectionaltersthegutmicrobiotabyinducinginappetence
AT johnstregoning respiratoryviralinfectionaltersthegutmicrobiotabyinducinginappetence
_version_ 1718427090126110720