Influenza A H1N1 Induced Disturbance of the Respiratory and Fecal Microbiome of German Landrace Pigs – a Multi-Omics Characterization
ABSTRACT Seasonal influenza outbreaks represent a large burden for the health care system as well as the economy. While the role of the microbiome has been elucidated in the context of various diseases, the impact of respiratory viral infections on the human microbiome is largely unknown. In this st...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2021-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/Spectrum.00182-21 |
| _version_ | 1818755104884391936 |
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| author | Laurin Christopher Gierse Alexander Meene Daniel Schultz Theresa Schwaiger Charlotte Schröder Pierre Mücke Daniela Zühlke Tjorven Hinzke Haitao Wang Karen Methling Bernd Kreikemeyer Jörg Bernhardt Dörte Becher Thomas C. Mettenleiter Michael Lalk Tim Urich Katharina Riedel |
| author_facet | Laurin Christopher Gierse Alexander Meene Daniel Schultz Theresa Schwaiger Charlotte Schröder Pierre Mücke Daniela Zühlke Tjorven Hinzke Haitao Wang Karen Methling Bernd Kreikemeyer Jörg Bernhardt Dörte Becher Thomas C. Mettenleiter Michael Lalk Tim Urich Katharina Riedel |
| author_sort | Laurin Christopher Gierse |
| collection | DOAJ |
| description | ABSTRACT Seasonal influenza outbreaks represent a large burden for the health care system as well as the economy. While the role of the microbiome has been elucidated in the context of various diseases, the impact of respiratory viral infections on the human microbiome is largely unknown. In this study, swine was used as an animal model to characterize the temporal dynamics of the respiratory and gastrointestinal microbiome in response to an influenza A virus (IAV) infection. A multi-omics approach was applied on fecal samples to identify alterations in microbiome composition and function during IAV infection. We observed significantly altered microbial richness and diversity in the gastrointestinal microbiome after IAV infection. In particular, increased abundances of Prevotellaceae were detected, while Clostridiaceae and Lachnospiraceae decreased. Moreover, our metaproteomics data indicated that the functional composition of the microbiome was heavily affected by the influenza infection. For instance, we identified decreased amounts of flagellin, correlating with reduced abundances of Lachnospiraceae and Clostridiaceae, possibly indicating involvement of a direct immune response toward flagellated Clostridia during IAV infection. Furthermore, enzymes involved in short-chain fatty acid (SCFA) synthesis were identified in higher abundances, while metabolome analyses revealed rather stable concentrations of SCFAs. In addition, 16S rRNA gene sequencing was used to characterize effects on the composition and natural development of the upper respiratory tract microbiome. Our results showed that IAV infection resulted in significant changes in the abundance of Moraxellaceae and Pasteurellaceae in the upper respiratory tract. Surprisingly, temporal development of the respiratory microbiome structure was not affected. IMPORTANCE Here, we used swine as a biomedical model to elucidate the impact of influenza A H1N1 infection on structure and function of the respiratory and gastrointestinal tract microbiome by employing a multi-omics analytical approach. To our knowledge, this is the first study to investigate the temporal development of the porcine microbiome and to provide insights into the functional capacity of the gastrointestinal microbiome during influenza A virus infection. |
| first_indexed | 2024-12-18T05:33:51Z |
| format | Article |
| id | doaj.art-d49a17c82c7545f982d46af9386f8fbd |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-18T05:33:51Z |
| publishDate | 2021-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-d49a17c82c7545f982d46af9386f8fbd2022-12-21T21:19:22ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972021-10-019210.1128/Spectrum.00182-21Influenza A H1N1 Induced Disturbance of the Respiratory and Fecal Microbiome of German Landrace Pigs – a Multi-Omics CharacterizationLaurin Christopher Gierse0Alexander Meene1Daniel Schultz2Theresa Schwaiger3Charlotte Schröder4Pierre Mücke5Daniela Zühlke6Tjorven Hinzke7Haitao Wang8Karen Methling9Bernd Kreikemeyer10Jörg Bernhardt11Dörte Becher12Thomas C. Mettenleiter13Michael Lalk14Tim Urich15Katharina Riedel16Institute of Microbiology, University of Greifswald, Greifswald, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyInstitute of Biochemistry, University of Greifswald, Greifswald, GermanyFriedrich-Loeffler-Institut, Greifswald-Insel Riems, Greifswald, GermanyFriedrich-Loeffler-Institut, Greifswald-Insel Riems, Greifswald, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyInstitute of Biochemistry, University of Greifswald, Greifswald, GermanyInstitute for Medical Microbiology, Virology and Hygiene, Rostock University Medical Centre, Rostock, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyFriedrich-Loeffler-Institut, Greifswald-Insel Riems, Greifswald, GermanyInstitute of Biochemistry, University of Greifswald, Greifswald, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyInstitute of Microbiology, University of Greifswald, Greifswald, GermanyABSTRACT Seasonal influenza outbreaks represent a large burden for the health care system as well as the economy. While the role of the microbiome has been elucidated in the context of various diseases, the impact of respiratory viral infections on the human microbiome is largely unknown. In this study, swine was used as an animal model to characterize the temporal dynamics of the respiratory and gastrointestinal microbiome in response to an influenza A virus (IAV) infection. A multi-omics approach was applied on fecal samples to identify alterations in microbiome composition and function during IAV infection. We observed significantly altered microbial richness and diversity in the gastrointestinal microbiome after IAV infection. In particular, increased abundances of Prevotellaceae were detected, while Clostridiaceae and Lachnospiraceae decreased. Moreover, our metaproteomics data indicated that the functional composition of the microbiome was heavily affected by the influenza infection. For instance, we identified decreased amounts of flagellin, correlating with reduced abundances of Lachnospiraceae and Clostridiaceae, possibly indicating involvement of a direct immune response toward flagellated Clostridia during IAV infection. Furthermore, enzymes involved in short-chain fatty acid (SCFA) synthesis were identified in higher abundances, while metabolome analyses revealed rather stable concentrations of SCFAs. In addition, 16S rRNA gene sequencing was used to characterize effects on the composition and natural development of the upper respiratory tract microbiome. Our results showed that IAV infection resulted in significant changes in the abundance of Moraxellaceae and Pasteurellaceae in the upper respiratory tract. Surprisingly, temporal development of the respiratory microbiome structure was not affected. IMPORTANCE Here, we used swine as a biomedical model to elucidate the impact of influenza A H1N1 infection on structure and function of the respiratory and gastrointestinal tract microbiome by employing a multi-omics analytical approach. To our knowledge, this is the first study to investigate the temporal development of the porcine microbiome and to provide insights into the functional capacity of the gastrointestinal microbiome during influenza A virus infection.https://journals.asm.org/doi/10.1128/Spectrum.00182-2116S rRNA gene sequencinginfluenza Amicrobiomebiomedical model swinemetabolomicsmetaproteomics |
| spellingShingle | Laurin Christopher Gierse Alexander Meene Daniel Schultz Theresa Schwaiger Charlotte Schröder Pierre Mücke Daniela Zühlke Tjorven Hinzke Haitao Wang Karen Methling Bernd Kreikemeyer Jörg Bernhardt Dörte Becher Thomas C. Mettenleiter Michael Lalk Tim Urich Katharina Riedel Influenza A H1N1 Induced Disturbance of the Respiratory and Fecal Microbiome of German Landrace Pigs – a Multi-Omics Characterization Microbiology Spectrum 16S rRNA gene sequencing influenza A microbiome biomedical model swine metabolomics metaproteomics |
| title | Influenza A H1N1 Induced Disturbance of the Respiratory and Fecal Microbiome of German Landrace Pigs – a Multi-Omics Characterization |
| title_full | Influenza A H1N1 Induced Disturbance of the Respiratory and Fecal Microbiome of German Landrace Pigs – a Multi-Omics Characterization |
| title_fullStr | Influenza A H1N1 Induced Disturbance of the Respiratory and Fecal Microbiome of German Landrace Pigs – a Multi-Omics Characterization |
| title_full_unstemmed | Influenza A H1N1 Induced Disturbance of the Respiratory and Fecal Microbiome of German Landrace Pigs – a Multi-Omics Characterization |
| title_short | Influenza A H1N1 Induced Disturbance of the Respiratory and Fecal Microbiome of German Landrace Pigs – a Multi-Omics Characterization |
| title_sort | influenza a h1n1 induced disturbance of the respiratory and fecal microbiome of german landrace pigs a multi omics characterization |
| topic | 16S rRNA gene sequencing influenza A microbiome biomedical model swine metabolomics metaproteomics |
| url | https://journals.asm.org/doi/10.1128/Spectrum.00182-21 |
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