Gut microbiome alterations and gut barrier dysfunction are associated with host immune homeostasis in COVID-19 patients

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Abstract

Background

COVID-19 is an infectious disease characterized by multiple respiratory and extrapulmonary manifestations, including gastrointestinal symptoms. Although recent studies have linked gut microbiota to infectious diseases such as influenza, little is known about the role of the gut microbiota in COVID-19 pathophysiology.

Methods

To better understand the host-gut microbiota interactions in COVID-19, we characterized the gut microbial community and gut barrier function using metagenomic and metaproteomic approaches in 63 COVID-19 patients and 8 non-infected controls. Both immunohematological parameters and transcriptional profiles were measured to reflect the immune response in COVID-19 patients.

Results

Altered gut microbial composition was observed in COVID-19 patients, which was characterized by decreased commensal species and increased opportunistic pathogenic species. Severe illness was associated with higher abundance of four microbial species (i.e., Burkholderia contaminans, Bacteroides nordii, Bifidobacterium longum, and Blautia sp. CAG 257), six microbial pathways (e.g., glycolysis and fermentation), and 10 virulence genes. These severity-related microbial features were further associated with host immune response. For example, the abundance of Bu. contaminans was associated with higher levels of inflammation biomarkers and lower levels of immune cells. Furthermore, human-origin proteins identified from both blood and fecal samples suggested gut barrier dysfunction in COVID-19 patients. The circulating levels of lipopolysaccharide-binding protein increased in patients with severe illness and were associated with circulating inflammation biomarkers and immune cells. Besides, proteins of disease-related bacteria (e.g., B. longum) were detectable in blood samples from patients.

Conclusions

Our results suggest that the dysbiosis of the gut microbiome and the dysfunction of the gut barrier might play a role in the pathophysiology of COVID-19 by affecting host immune homeostasis.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12916-021-02212-0.

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Most cited references 55

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Trimmomatic: a flexible trimmer for Illumina sequence data

Anthony M. Bolger, Marc Lohse, Bjoern Usadel (2014)

Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.

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Fast gapped-read alignment with Bowtie 2.

Ben Langmead, Steven L Salzberg (2022)

As the rate of sequencing increases, greater throughput is demanded from read aligners. The full-text minute index is often used to make alignment very fast and memory-efficient, but the approach is ill-suited to finding longer, gapped alignments. Bowtie 2 combines the strengths of the full-text minute index with the flexibility and speed of hardware-accelerated dynamic programming algorithms to achieve a combination of high speed, sensitivity and accuracy.

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A new coronavirus associated with human respiratory disease in China

Fan Wu, Su Zhao, Bin Yu … (2020)

Emerging infectious diseases, such as severe acute respiratory syndrome (SARS) and Zika virus disease, present a major threat to public health 1–3 . Despite intense research efforts, how, when and where new diseases appear are still a source of considerable uncertainty. A severe respiratory disease was recently reported in Wuhan, Hubei province, China. As of 25 January 2020, at least 1,975 cases had been reported since the first patient was hospitalized on 12 December 2019. Epidemiological investigations have suggested that the outbreak was associated with a seafood market in Wuhan. Here we study a single patient who was a worker at the market and who was admitted to the Central Hospital of Wuhan on 26 December 2019 while experiencing a severe respiratory syndrome that included fever, dizziness and a cough. Metagenomic RNA sequencing 4 of a sample of bronchoalveolar lavage fluid from the patient identified a new RNA virus strain from the family Coronaviridae, which is designated here ‘WH-Human 1’ coronavirus (and has also been referred to as ‘2019-nCoV’). Phylogenetic analysis of the complete viral genome (29,903 nucleotides) revealed that the virus was most closely related (89.1% nucleotide similarity) to a group of SARS-like coronaviruses (genus Betacoronavirus, subgenus Sarbecovirus) that had previously been found in bats in China 5 . This outbreak highlights the ongoing ability of viral spill-over from animals to cause severe disease in humans.

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Author and article information

Contributors

Yan Zheng:

ORCID: http://orcid.org/0000-0003-1129-3147

yan_zheng@fudan.edu.cn

Yan-Mei Chen: chenyanmei@shphc.org.cn

Journal

Journal ID (nlm-ta): BMC Med

Journal ID (iso-abbrev): BMC Med

Title: BMC Medicine

Publisher: BioMed Central (London )

ISSN (Electronic): 1741-7015

Publication date (Electronic): 20 January 2022

Publication date PMC-release: 20 January 2022

Publication date Collection: 2022

Volume: 20

Electronic Location Identifier: 24

Affiliations

[1 ]GRID grid.8547.e, ISNI 0000 0001 0125 2443, State Key Laboratory of Genetic Engineering, School of Life Sciences and Human Phenome Institute, , Fudan University, ; Shanghai, China

[2 ]GRID grid.8547.e, ISNI 0000 0001 0125 2443, Shanghai Public Health Clinical Center, State Key Laboratory of Genetic Engineering, School of Life Sciences and Human Phenome Institute, , Fudan University, ; Shanghai, China

Author information

Yan Zheng http://orcid.org/0000-0003-1129-3147

Article

Publisher ID: 2212

DOI: 10.1186/s12916-021-02212-0

PMC ID: 8769945

PubMed ID: 35045853

SO-VID: 5dc1bc86-31f3-4e06-af16-89e95ec5ba26

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 12 September 2021

Date accepted : 9 December 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003399, Science and Technology Commission of Shanghai Municipality;

Award ID: 2017SHZDZX01

Funded by: Science and Technology Commission of Shanghai Municipality for International Partnership Project

Award ID: 20490780100

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 31741072

Award ID: 81973032

Award ID: 32041004

Award ID: 31930001

Award ID: 3213000167

Custom metadata

ScienceOpen disciplines: Medicine

Keywords: covid-19,sars-cov-2,microbiome,metaproteomic,gut barrier,immune homeostasis

Data availability:

ScienceOpen disciplines: Medicine

Keywords: covid-19, sars-cov-2, microbiome, metaproteomic, gut barrier, immune homeostasis

Gut microbiome alterations and gut barrier dysfunction are associated with host immune homeostasis in COVID-19 patients

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Abstract

Background

Methods

Results

Conclusions

Supplementary Information

Related collections

Novel Coronavirus Disease COVID-19

Most cited references 55

Trimmomatic: a flexible trimmer for Illumina sequence data

Fast gapped-read alignment with Bowtie 2.

A new coronavirus associated with human respiratory disease in China

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Contributors

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