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Airway bacterial and fungal microbiome in chronic obstructive pulmonary disease

Haiyue Liu, Zhenyu Liang, Nannan Cao, Xilan Tan, Zuheng Liu, Fengyan Wang, Yuqiong Yang, Chunxi Li, Yan He, Jin Su, Rongchang Chen, Zhang Wang, Hongwei Zhou
doi: https://doi.org/10.1101/2020.10.05.327536
Haiyue Liu
1State Key Laboratory of Organ Failure Research, Division of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, China
2Microbiome Medicine Center, Zhujiang Hospital, Southern Medical University, Guangzhou, China
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Zhenyu Liang
3State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, China
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Nannan Cao
1State Key Laboratory of Organ Failure Research, Division of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, China
2Microbiome Medicine Center, Zhujiang Hospital, Southern Medical University, Guangzhou, China
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Xilan Tan
1State Key Laboratory of Organ Failure Research, Division of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, China
2Microbiome Medicine Center, Zhujiang Hospital, Southern Medical University, Guangzhou, China
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Zuheng Liu
4State Key Laboratory of Organ Failure Research, Department of Cardiology, Nanfang Hospital, Southern Medical University, Guangzhou, China
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Fengyan Wang
3State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, China
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Yuqiong Yang
3State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, China
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Chunxi Li
5Chronic Airways Diseases Laboratory, Department of Respiratory and Critical Care Medicine, Nanfang Hospital, Southern Medical University, Guangzhou, China
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Yan He
1State Key Laboratory of Organ Failure Research, Division of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, China
2Microbiome Medicine Center, Zhujiang Hospital, Southern Medical University, Guangzhou, China
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Jin Su
5Chronic Airways Diseases Laboratory, Department of Respiratory and Critical Care Medicine, Nanfang Hospital, Southern Medical University, Guangzhou, China
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Rongchang Chen
3State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, China
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Zhang Wang
2Microbiome Medicine Center, Zhujiang Hospital, Southern Medical University, Guangzhou, China
6Institute of Ecological Science, School of Life Science, South China Normal University, Guangzhou, China
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  • For correspondence: biodegradation@gmail.com wangz@m.scnu.edu.cn
Hongwei Zhou
1State Key Laboratory of Organ Failure Research, Division of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, China
2Microbiome Medicine Center, Zhujiang Hospital, Southern Medical University, Guangzhou, China
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  • For correspondence: biodegradation@gmail.com wangz@m.scnu.edu.cn
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Abstract

Background Little is known about airway mycobiome, and its relationship with bacterial microbiome in chronic obstructive pulmonary disease (COPD).

Methods Here we report the first simultaneous characterization of sputum bacterial and fungal microbiome in 84 stable COPD and 29 healthy subjects, using 16S ribosomal DNA and fungal internal transcribed spacer DNA sequencing.

Results Ascomycota predominated over Basidiomycota in fungal microbiome both in COPD patients and healthy controls. Meyerozyma, Candida, Aspergillus and Schizophyllum were most abundant at the genus level. There was a significant inverse correlation between bacterial and fungal microbial diversity, both of which altered in opposite directions in COPD patients versus controls, and in frequent versus non-frequent exacerbators. An enhanced bacterial-fungal ecological interaction was observed in COPD patients, which was characterized by higher proportion of co-occurrence intrakingdom interactions and co-exclusive interkingdom interactions. In COPD, four mutually co-occurring fungal operational taxonomic units (OTUs) in Candida palmioleophila, Aspergillus and Sordariomycetes exhibited co-exclusive relationships with other fungal OTUs, which was specifically present in frequent exacerbators but not in non-frequent exacerbators. Conversely, the mutual co-occurrence interactions between bacterial OTUs in Rothia mucilaginosa, Streptococcus, Veillonella and Prevotella, showed up in non-frequent exacerbators but not in frequent exacerbators. The perturbed bacterial-fungal interactions in COPD were associated with increased airway inflammatory mediators such as IL-6 and IL-8.

Interpretation The disruption of airway bacterial-fungal community balance, characterized by the loss of commensal bacterial taxa and enriched pathogenic fungal taxa, is implicated in COPD. The airway mycobiome is an important cofactor mediating COPD pathogenic infection and host inflammation.

Clinical Trial Registration www.clinicaltrials.gov (NCT 03240315).

Footnotes

  • Abbreviation List: AUC: Area under the curve; COPD: Chronic obstructive pulmonary disease; ENA: European Nucleotide Archive; FDR: False discovery rate; FEV1: Forced expiratory volume in 1 s; FVC: Forced vital capacity; GOLD: Global Initiative for Chronic Obstructive Lung Disease; LDA: Linear discriminant analysis; LEfSe: Linear discriminant analysis effect size; IL: Interleukin; INF-γ: Interferon-γ; OTUs: Operational taxonomic units; PBS: phosphate-buffered saline; PCoA: Principal Coordinate Analysis; QIIME: Quantitative Insights into Microbial Ecology; sRAGE: Soluble receptor for advanced glycation endproducts; TGF-β: Transforming growth factor-β; TNF-α: Tumor necrosis factor α; VEGF: Vascular endothelial growth factor

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 06, 2020.
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Airway bacterial and fungal microbiome in chronic obstructive pulmonary disease
Haiyue Liu, Zhenyu Liang, Nannan Cao, Xilan Tan, Zuheng Liu, Fengyan Wang, Yuqiong Yang, Chunxi Li, Yan He, Jin Su, Rongchang Chen, Zhang Wang, Hongwei Zhou
bioRxiv 2020.10.05.327536; doi: https://doi.org/10.1101/2020.10.05.327536
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Airway bacterial and fungal microbiome in chronic obstructive pulmonary disease
Haiyue Liu, Zhenyu Liang, Nannan Cao, Xilan Tan, Zuheng Liu, Fengyan Wang, Yuqiong Yang, Chunxi Li, Yan He, Jin Su, Rongchang Chen, Zhang Wang, Hongwei Zhou
bioRxiv 2020.10.05.327536; doi: https://doi.org/10.1101/2020.10.05.327536

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