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Influenza A virus infection impacts systemic microbiota dynamics and causes quantitative enteric dysbiosis.
Microbiome. 2018 01 10; 6(1):9.M

Abstract

BACKGROUND

Microbiota integrity is essential for a growing number of physiological processes. Consequently, disruption of microbiota homeostasis correlates with a variety of pathological states. Importantly, commensal microbiota provide a shield against invading bacterial pathogens, probably by direct competition. The impact of viral infections on host microbiota composition and dynamics is poorly understood. Influenza A viruses (IAV) are common respiratory pathogens causing acute infections. Here, we show dynamic changes in respiratory and intestinal microbiota over the course of a sublethal IAV infection in a mouse model.

RESULTS

Using a combination of 16S rRNA gene-specific next generation sequencing and qPCR as well as culturing of bacterial organ content, we found body site-specific and transient microbiota responses. In the lower respiratory tract, we observed only minor qualitative changes in microbiota composition. No quantitative impact on bacterial colonization after IAV infection was detectable, despite a robust antimicrobial host response and increased sensitivity to bacterial super infection. In contrast, in the intestine, IAV induced robust depletion of bacterial content, disruption of mucus layer integrity, and higher levels of antimicrobial peptides in Paneth cells. As a functional consequence of IAV-mediated microbiota depletion, we demonstrated that the small intestine is rendered more susceptible to bacterial pathogen invasion, in a Salmonella typhimurium super infection model.

CONCLUSION

We show for the first time the consequences of IAV infection for lower respiratory tract and intestinal microbiobiota in a qualitative and quantitative fashion. The discrepancy of relative 16S rRNA gene next-generation sequencing (NGS) and normalized 16S rRNA gene-specific qPCR stresses the importance of combining qualitative and quantitative approaches to correctly analyze composition of organ associated microbial communities. The transiently induced dysbiosis underlines the overall stability of microbial communities to effects of acute infection. However, during a short-time window, specific ecological niches might lose their microbiota shield and remain vulnerable to bacterial invasion.

Authors+Show Affiliations

Department of Microbiology and Molecular Medicine, University Medical Center (CMU), University of Geneva, Rue Michel-Servet 1, CH-1211, Geneva, Switzerland.Department of Microbiology and Molecular Medicine, University Medical Center (CMU), University of Geneva, Rue Michel-Servet 1, CH-1211, Geneva, Switzerland.Department of Microbiology, University of Chicago, Chicago, IL, 60637, USA.Department of Microbiology, University of Chicago, Chicago, IL, 60637, USA.Department of Microbiology and Molecular Medicine, University Medical Center (CMU), University of Geneva, Rue Michel-Servet 1, CH-1211, Geneva, Switzerland. mirco.schmolke@unige.ch.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29321057

Citation

Yildiz, Soner, et al. "Influenza a Virus Infection Impacts Systemic Microbiota Dynamics and Causes Quantitative Enteric Dysbiosis." Microbiome, vol. 6, no. 1, 2018, p. 9.
Yildiz S, Mazel-Sanchez B, Kandasamy M, et al. Influenza A virus infection impacts systemic microbiota dynamics and causes quantitative enteric dysbiosis. Microbiome. 2018;6(1):9.
Yildiz, S., Mazel-Sanchez, B., Kandasamy, M., Manicassamy, B., & Schmolke, M. (2018). Influenza A virus infection impacts systemic microbiota dynamics and causes quantitative enteric dysbiosis. Microbiome, 6(1), 9. https://doi.org/10.1186/s40168-017-0386-z
Yildiz S, et al. Influenza a Virus Infection Impacts Systemic Microbiota Dynamics and Causes Quantitative Enteric Dysbiosis. Microbiome. 2018 01 10;6(1):9. PubMed PMID: 29321057.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Influenza A virus infection impacts systemic microbiota dynamics and causes quantitative enteric dysbiosis. AU - Yildiz,Soner, AU - Mazel-Sanchez,Béryl, AU - Kandasamy,Matheswaran, AU - Manicassamy,Balaji, AU - Schmolke,Mirco, Y1 - 2018/01/10/ PY - 2017/09/08/received PY - 2017/12/14/accepted PY - 2018/1/12/entrez PY - 2018/1/13/pubmed PY - 2018/10/27/medline SP - 9 EP - 9 JF - Microbiome JO - Microbiome VL - 6 IS - 1 N2 - BACKGROUND: Microbiota integrity is essential for a growing number of physiological processes. Consequently, disruption of microbiota homeostasis correlates with a variety of pathological states. Importantly, commensal microbiota provide a shield against invading bacterial pathogens, probably by direct competition. The impact of viral infections on host microbiota composition and dynamics is poorly understood. Influenza A viruses (IAV) are common respiratory pathogens causing acute infections. Here, we show dynamic changes in respiratory and intestinal microbiota over the course of a sublethal IAV infection in a mouse model. RESULTS: Using a combination of 16S rRNA gene-specific next generation sequencing and qPCR as well as culturing of bacterial organ content, we found body site-specific and transient microbiota responses. In the lower respiratory tract, we observed only minor qualitative changes in microbiota composition. No quantitative impact on bacterial colonization after IAV infection was detectable, despite a robust antimicrobial host response and increased sensitivity to bacterial super infection. In contrast, in the intestine, IAV induced robust depletion of bacterial content, disruption of mucus layer integrity, and higher levels of antimicrobial peptides in Paneth cells. As a functional consequence of IAV-mediated microbiota depletion, we demonstrated that the small intestine is rendered more susceptible to bacterial pathogen invasion, in a Salmonella typhimurium super infection model. CONCLUSION: We show for the first time the consequences of IAV infection for lower respiratory tract and intestinal microbiobiota in a qualitative and quantitative fashion. The discrepancy of relative 16S rRNA gene next-generation sequencing (NGS) and normalized 16S rRNA gene-specific qPCR stresses the importance of combining qualitative and quantitative approaches to correctly analyze composition of organ associated microbial communities. The transiently induced dysbiosis underlines the overall stability of microbial communities to effects of acute infection. However, during a short-time window, specific ecological niches might lose their microbiota shield and remain vulnerable to bacterial invasion. SN - 2049-2618 UR - https://www.unboundmedicine.com/medline/citation/29321057/Influenza_A_virus_infection_impacts_systemic_microbiota_dynamics_and_causes_quantitative_enteric_dysbiosis_ L2 - https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-017-0386-z DB - PRIME DP - Unbound Medicine ER -