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Impact of Pneumococcal and Viral Pneumonia on the Respiratory and Intestinal Tract Microbiomes of Mice

With 2.56 million deaths worldwide annually, pneumonia is one of the leading causes of death. The most frequent causative pathogens are Streptococcus pneumoniae and influenza A virus. Lately, the interaction between the pathogens, the host, and its microbiome have gained more attention. The microbio...

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Autores principales: Gierse, Laurin Christopher, Meene, Alexander, Skorka, Sebastian, Cuypers, Fabian, Surabhi, Surabhi, Ferrero-Bordera, Borja, Kreikemeyer, Bernd, Becher, Dörte, Hammerschmidt, Sven, Siemens, Nikolai, Urich, Tim, Riedel, Katharina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269894/
https://www.ncbi.nlm.nih.gov/pubmed/36988458
http://dx.doi.org/10.1128/spectrum.03447-22
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author Gierse, Laurin Christopher
Meene, Alexander
Skorka, Sebastian
Cuypers, Fabian
Surabhi, Surabhi
Ferrero-Bordera, Borja
Kreikemeyer, Bernd
Becher, Dörte
Hammerschmidt, Sven
Siemens, Nikolai
Urich, Tim
Riedel, Katharina
author_facet Gierse, Laurin Christopher
Meene, Alexander
Skorka, Sebastian
Cuypers, Fabian
Surabhi, Surabhi
Ferrero-Bordera, Borja
Kreikemeyer, Bernd
Becher, Dörte
Hammerschmidt, Sven
Siemens, Nikolai
Urich, Tim
Riedel, Katharina
author_sort Gierse, Laurin Christopher
collection PubMed
description With 2.56 million deaths worldwide annually, pneumonia is one of the leading causes of death. The most frequent causative pathogens are Streptococcus pneumoniae and influenza A virus. Lately, the interaction between the pathogens, the host, and its microbiome have gained more attention. The microbiome is known to promote the immune response toward pathogens; however, our knowledge on how infections affect the microbiome is still scarce. Here, the impact of colonization and infection with S. pneumoniae and influenza A virus on the structure and function of the respiratory and gastrointestinal microbiomes of mice was investigated. Using a meta-omics approach, we identified specific differences between the bacterial and viral infection. Pneumococcal colonization had minor effects on the taxonomic composition of the respiratory microbiome, while acute infections caused decreased microbial complexity. In contrast, richness was unaffected following H1N1 infection. Within the gastrointestinal microbiome, we found exclusive changes in structure and function, depending on the pathogen. While pneumococcal colonization had no effects on taxonomic composition of the gastrointestinal microbiome, increased abundance of Akkermansiaceae and Spirochaetaceae as well as decreased amounts of Clostridiaceae were exclusively found during invasive S. pneumoniae infection. The presence of Staphylococcaceae was specific for viral pneumonia. Investigation of the intestinal microbiomés functional composition revealed reduced expression of flagellin and rubrerythrin and increased levels of ATPase during pneumococcal infection, while increased amounts of acetyl coenzyme A (acetyl-CoA) acetyltransferase and enoyl-CoA transferase were unique after H1N1 infection. In conclusion, identification of specific taxonomic and functional profiles of the respiratory and gastrointestinal microbiome allowed the discrimination between bacterial and viral pneumonia. IMPORTANCE Pneumonia is one of the leading causes of death worldwide. Here, we compared the impact of bacterial- and viral-induced pneumonia on the respiratory and gastrointestinal microbiome. Using a meta-omics approach, we identified specific profiles that allow discrimination between bacterial and viral causative.
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spelling pubmed-102698942023-06-16 Impact of Pneumococcal and Viral Pneumonia on the Respiratory and Intestinal Tract Microbiomes of Mice Gierse, Laurin Christopher Meene, Alexander Skorka, Sebastian Cuypers, Fabian Surabhi, Surabhi Ferrero-Bordera, Borja Kreikemeyer, Bernd Becher, Dörte Hammerschmidt, Sven Siemens, Nikolai Urich, Tim Riedel, Katharina Microbiol Spectr Research Article With 2.56 million deaths worldwide annually, pneumonia is one of the leading causes of death. The most frequent causative pathogens are Streptococcus pneumoniae and influenza A virus. Lately, the interaction between the pathogens, the host, and its microbiome have gained more attention. The microbiome is known to promote the immune response toward pathogens; however, our knowledge on how infections affect the microbiome is still scarce. Here, the impact of colonization and infection with S. pneumoniae and influenza A virus on the structure and function of the respiratory and gastrointestinal microbiomes of mice was investigated. Using a meta-omics approach, we identified specific differences between the bacterial and viral infection. Pneumococcal colonization had minor effects on the taxonomic composition of the respiratory microbiome, while acute infections caused decreased microbial complexity. In contrast, richness was unaffected following H1N1 infection. Within the gastrointestinal microbiome, we found exclusive changes in structure and function, depending on the pathogen. While pneumococcal colonization had no effects on taxonomic composition of the gastrointestinal microbiome, increased abundance of Akkermansiaceae and Spirochaetaceae as well as decreased amounts of Clostridiaceae were exclusively found during invasive S. pneumoniae infection. The presence of Staphylococcaceae was specific for viral pneumonia. Investigation of the intestinal microbiomés functional composition revealed reduced expression of flagellin and rubrerythrin and increased levels of ATPase during pneumococcal infection, while increased amounts of acetyl coenzyme A (acetyl-CoA) acetyltransferase and enoyl-CoA transferase were unique after H1N1 infection. In conclusion, identification of specific taxonomic and functional profiles of the respiratory and gastrointestinal microbiome allowed the discrimination between bacterial and viral pneumonia. IMPORTANCE Pneumonia is one of the leading causes of death worldwide. Here, we compared the impact of bacterial- and viral-induced pneumonia on the respiratory and gastrointestinal microbiome. Using a meta-omics approach, we identified specific profiles that allow discrimination between bacterial and viral causative. American Society for Microbiology 2023-03-29 /pmc/articles/PMC10269894/ /pubmed/36988458 http://dx.doi.org/10.1128/spectrum.03447-22 Text en Copyright © 2023 Gierse et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Gierse, Laurin Christopher
Meene, Alexander
Skorka, Sebastian
Cuypers, Fabian
Surabhi, Surabhi
Ferrero-Bordera, Borja
Kreikemeyer, Bernd
Becher, Dörte
Hammerschmidt, Sven
Siemens, Nikolai
Urich, Tim
Riedel, Katharina
Impact of Pneumococcal and Viral Pneumonia on the Respiratory and Intestinal Tract Microbiomes of Mice
title Impact of Pneumococcal and Viral Pneumonia on the Respiratory and Intestinal Tract Microbiomes of Mice
title_full Impact of Pneumococcal and Viral Pneumonia on the Respiratory and Intestinal Tract Microbiomes of Mice
title_fullStr Impact of Pneumococcal and Viral Pneumonia on the Respiratory and Intestinal Tract Microbiomes of Mice
title_full_unstemmed Impact of Pneumococcal and Viral Pneumonia on the Respiratory and Intestinal Tract Microbiomes of Mice
title_short Impact of Pneumococcal and Viral Pneumonia on the Respiratory and Intestinal Tract Microbiomes of Mice
title_sort impact of pneumococcal and viral pneumonia on the respiratory and intestinal tract microbiomes of mice
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10269894/
https://www.ncbi.nlm.nih.gov/pubmed/36988458
http://dx.doi.org/10.1128/spectrum.03447-22
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