Transcriptionally Active Lung Microbiome and Its Association with Bacterial Biomass and Host Inflammatory Status

ABSTRACT Alteration of the lung microbiome has been observed in several respiratory tract diseases. However, most previous studies were based on 16S ribosomal RNA and shotgun metagenome sequencing; the viability and functional activity of the microbiome, as well as its interaction with host immune s...

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Autores principales: Lili Ren, Rongbao Zhang, Jian Rao, Yan Xiao, Zhao Zhang, Bin Yang, Depan Cao, Hui Zhong, Pu Ning, Ying Shang, Mingkun Li, Zhancheng Gao, Jianwei Wang
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:db827d55bb7d4691be0effae7a5259f12021-12-02T19:47:34ZTranscriptionally Active Lung Microbiome and Its Association with Bacterial Biomass and Host Inflammatory Status10.1128/mSystems.00199-182379-5077https://doaj.org/article/db827d55bb7d4691be0effae7a5259f12018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00199-18https://doaj.org/toc/2379-5077ABSTRACT Alteration of the lung microbiome has been observed in several respiratory tract diseases. However, most previous studies were based on 16S ribosomal RNA and shotgun metagenome sequencing; the viability and functional activity of the microbiome, as well as its interaction with host immune systems, have not been well studied. To characterize the active lung microbiome and its associations with host immune response and clinical features, we applied metatranscriptome sequencing to bronchoalveolar lavage fluid (BALF) samples from 25 patients with chronic obstructive pulmonary disease (COPD) and from nine control cases without known pulmonary disease. Community structure analyses revealed three distinct microbial compositions, which were significantly correlated with bacterial biomass, human Th17 immune response, and COPD exacerbation frequency. Specifically, samples with transcriptionally active Streptococcus, Rothia, or Pseudomonas had bacterial loads 16 times higher than samples enriched for Escherichia and Ralstonia. These high-bacterial-load samples also tended to undergo a stronger Th17 immune response. Furthermore, an increased proportion of lymphocytes was found in samples with active Pseudomonas. In addition, COPD patients with active Streptococcus or Rothia infections tended to have lower rates of exacerbations than patients with active Pseudomonas and patients with lower bacterial biomass. Our results support the idea of a stratified structure of the active lung microbiome and a significant host-microbe interaction. We speculate that diverse lung microbiomes exist in the population and that their presence and activities could either influence or reflect different aspects of lung health. IMPORTANCE Recent studies of the microbiome proposed that resident microbes play a beneficial role in maintaining human health. Although lower respiratory tract disease is a leading cause of sickness and mortality, how the lung microbiome interacts with human health remains largely unknown. Here we assessed the association between the lung microbiome and host gene expression, cytokine concentration, and over 20 clinical features. Intriguingly, we found a stratified structure of the active lung microbiome which was significantly associated with bacterial biomass, lymphocyte proportion, human Th17 immune response, and COPD exacerbation frequency. These observations suggest that the microbiome plays a significant role in lung homeostasis. Not only microbial composition but also active functional elements and host immunity characteristics differed among different individuals. Such diversity may partially account for the variation in susceptibility to particular diseases.Lili RenRongbao ZhangJian RaoYan XiaoZhao ZhangBin YangDepan CaoHui ZhongPu NingYing ShangMingkun LiZhancheng GaoJianwei WangAmerican Society for Microbiologyarticleairborne microorganismsbacterial biomasslung microbiomelung microbiotametatranscriptomemicrobial communitiesMicrobiologyQR1-502ENmSystems, Vol 3, Iss 5 (2018)
institution DOAJ
collection DOAJ
language EN
topic airborne microorganisms
bacterial biomass
lung microbiome
lung microbiota
metatranscriptome
microbial communities
Microbiology
QR1-502
spellingShingle airborne microorganisms
bacterial biomass
lung microbiome
lung microbiota
metatranscriptome
microbial communities
Microbiology
QR1-502
Lili Ren
Rongbao Zhang
Jian Rao
Yan Xiao
Zhao Zhang
Bin Yang
Depan Cao
Hui Zhong
Pu Ning
Ying Shang
Mingkun Li
Zhancheng Gao
Jianwei Wang
Transcriptionally Active Lung Microbiome and Its Association with Bacterial Biomass and Host Inflammatory Status
description ABSTRACT Alteration of the lung microbiome has been observed in several respiratory tract diseases. However, most previous studies were based on 16S ribosomal RNA and shotgun metagenome sequencing; the viability and functional activity of the microbiome, as well as its interaction with host immune systems, have not been well studied. To characterize the active lung microbiome and its associations with host immune response and clinical features, we applied metatranscriptome sequencing to bronchoalveolar lavage fluid (BALF) samples from 25 patients with chronic obstructive pulmonary disease (COPD) and from nine control cases without known pulmonary disease. Community structure analyses revealed three distinct microbial compositions, which were significantly correlated with bacterial biomass, human Th17 immune response, and COPD exacerbation frequency. Specifically, samples with transcriptionally active Streptococcus, Rothia, or Pseudomonas had bacterial loads 16 times higher than samples enriched for Escherichia and Ralstonia. These high-bacterial-load samples also tended to undergo a stronger Th17 immune response. Furthermore, an increased proportion of lymphocytes was found in samples with active Pseudomonas. In addition, COPD patients with active Streptococcus or Rothia infections tended to have lower rates of exacerbations than patients with active Pseudomonas and patients with lower bacterial biomass. Our results support the idea of a stratified structure of the active lung microbiome and a significant host-microbe interaction. We speculate that diverse lung microbiomes exist in the population and that their presence and activities could either influence or reflect different aspects of lung health. IMPORTANCE Recent studies of the microbiome proposed that resident microbes play a beneficial role in maintaining human health. Although lower respiratory tract disease is a leading cause of sickness and mortality, how the lung microbiome interacts with human health remains largely unknown. Here we assessed the association between the lung microbiome and host gene expression, cytokine concentration, and over 20 clinical features. Intriguingly, we found a stratified structure of the active lung microbiome which was significantly associated with bacterial biomass, lymphocyte proportion, human Th17 immune response, and COPD exacerbation frequency. These observations suggest that the microbiome plays a significant role in lung homeostasis. Not only microbial composition but also active functional elements and host immunity characteristics differed among different individuals. Such diversity may partially account for the variation in susceptibility to particular diseases.
format article
author Lili Ren
Rongbao Zhang
Jian Rao
Yan Xiao
Zhao Zhang
Bin Yang
Depan Cao
Hui Zhong
Pu Ning
Ying Shang
Mingkun Li
Zhancheng Gao
Jianwei Wang
author_facet Lili Ren
Rongbao Zhang
Jian Rao
Yan Xiao
Zhao Zhang
Bin Yang
Depan Cao
Hui Zhong
Pu Ning
Ying Shang
Mingkun Li
Zhancheng Gao
Jianwei Wang
author_sort Lili Ren
title Transcriptionally Active Lung Microbiome and Its Association with Bacterial Biomass and Host Inflammatory Status
title_short Transcriptionally Active Lung Microbiome and Its Association with Bacterial Biomass and Host Inflammatory Status
title_full Transcriptionally Active Lung Microbiome and Its Association with Bacterial Biomass and Host Inflammatory Status
title_fullStr Transcriptionally Active Lung Microbiome and Its Association with Bacterial Biomass and Host Inflammatory Status
title_full_unstemmed Transcriptionally Active Lung Microbiome and Its Association with Bacterial Biomass and Host Inflammatory Status
title_sort transcriptionally active lung microbiome and its association with bacterial biomass and host inflammatory status
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/db827d55bb7d4691be0effae7a5259f1
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