Limited Impact of SARS-CoV-2 on the Human Naso-Oropharyngeal Microbiota in Hospitalized Patients

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Reviewed Marked as Reviewed by Svetlana up on 2024-7-5
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
Authors
Lai CKC, Cheung MK, Lui GCY, Ling L, Chan JYK, Ng RWY, Chan HC, Yeung ACM, Ho WCS, Boon SS, Chan PKS, Chen Z
Journal
Microbiology spectrum
Year
2022
Keywords:
16S rRNA, COVID-19, SARS-CoV-2, hospitalized, naso-oropharyngeal microbiome
Numerous studies have reported dysbiosis in the naso- and/or oro-pharyngeal microbiota of COVID-19 patients compared with healthy individuals; however, only a few small-scale studies have also included a disease control group. In this study, we characterized and compared the bacterial communities of pooled nasopharyngeal and throat swabs from hospitalized COVID-19 patients (n = 76), hospitalized non-COVID-19 patients with respiratory symptoms or related illnesses (n = 69), and local community controls (n = 76) using 16S rRNA gene V3-V4 amplicon sequencing. None of the subjects received antimicrobial therapy within 2 weeks prior to sample collection. Both COVID-19 and non-COVID-19 hospitalized patients differed in the composition, alpha and beta diversity, and metabolic potential of the naso-oropharyngeal microbiota compared with local controls. However, the microbial communities in the two hospitalized patient groups did not differ significantly from each other. Differential abundance analysis revealed the enrichment of nine bacterial genera in the COVID-19 patients compared with local controls; however, six of them were also enriched in the non-COVID-19 patients. Bacterial genera uniquely enriched in the COVID-19 patients included Alloprevotella and Solobacterium. In contrast, Mogibacterium and Lactococcus were dramatically decreased in COVID-19 patients only. Association analysis revealed that Alloprevotella in COVID-19 patients was positively correlated with the level of the inflammation biomarker C-reactive protein. Our findings reveal a limited impact of SARS-CoV-2 on the naso-oropharyngeal microbiota in hospitalized patients and suggest that Alloprevotella and Solobacterium are more specific biomarkers for COVID-19 detection. IMPORTANCE Our results showed that while both COVID-19 and non-COVID-19 hospitalized patients differed in the composition, alpha and beta diversity, and metabolic potential of the naso-oropharyngeal microbiota compared with local controls, the microbial communities in the two hospitalized patient groups did not differ significantly from each other, indicating a limited impact of SARS-CoV-2 on the naso-oropharyngeal microbiota in hospitalized patients. Besides, we identified Alloprevotella and Solobacterium as bacterial genera uniquely enriched in COVID-19 patients, which may serve as more specific biomarkers for COVID-19 detection.

Experiment 1


Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/14

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako

Subjects

Location of subjects
China
Host species Species from which microbiome was sampled. Contact us to have more species added.
Homo sapiens
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Nasopharynx , Throat Nasenrachenraum,Epipharynx,Nasal part of pharynx,Pars nasalis pharyngis,Rhinopharynx,Nasopharynx,nasopharynx,Gula,Throat,throat
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
COVID-19 2019 novel coronavirus,2019 novel coronavirus infection,2019-nCoV,2019-nCoV infection,beta-CoV,beta-CoVs,betacoronavirus,coronavirus disease 2019,SARS-coronavirus 2,SARS-CoV-2,severe acute respiratory syndrome coronavirus 2,severe acute respiratory syndrome coronavirus 2 infectious disease,β-coronavirus,β-CoV,β-CoVs,COVID-19,cOVID-19
Group 0 name Corresponds to the control (unexposed) group for case-control studies
local controls
Group 1 name Corresponds to the case (exposed) group for case-control studies
COVID-19 patients
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Hospitalized COVID-19 patients
Group 0 sample size Number of subjects in the control (unexposed) group
76
Group 1 sample size Number of subjects in the case (exposed) group
76
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
2 weeks

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V3-V4
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
relative abundances
Statistical test
LEfSe
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.05
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
Yes
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Richness Number of species
decreased

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/14

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Fig 2A

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized COVID-19 patients versus local controls.

Abundance in Group 1: increased abundance in COVID-19 patients

NCBI Quality ControlLinks
Actinomyces
Alloprevotella
Atopobium
Megasphaera
Prevotella
Solobacterium
Sphingomonas
Veillonella
Prevotella_7Prevotella_7

Revision editor(s): Abiola-Salako, Scholastica

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/18

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Fig 2A

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized COVID-19 patients versus local controls.

Abundance in Group 1: decreased abundance in COVID-19 patients

NCBI Quality ControlLinks
Actinobacillus
Alysiella
Bacteroides
Bifidobacterium
Blautia
Capnocytophaga
Catonella
Escherichia/Shigella sp.
Faecalibacterium
Filifactor
Finegoldia
Gemella
Haemophilus
Lactococcus
Lautropia
Lawsonella
Lentimicrobium
Mogibacterium
Neisseria
Oribacterium
Ruminococcus
Tannerella
Treponema
F0058F0058

Revision editor(s): Abiola-Salako, Scholastica

Experiment 2


Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/18

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Abnormality of the respiratory system Respiratory abnormality,Abnormality of the respiratory system,abnormality of the respiratory system
Group 1 name Corresponds to the case (exposed) group for case-control studies
Non-Covid-19 Patients
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Hospitalized non-COVID-19 patients with respiratory symptoms or related illnesses.
Group 1 sample size Number of subjects in the case (exposed) group
69

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
decreased
Richness Number of species
decreased

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/18

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Fig 2B

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized non-COVID-19 patients versus local controls.

Abundance in Group 1: increased abundance in Non-Covid-19 Patients

NCBI Quality ControlLinks
Actinomyces
Atopobium
Dolosigranulum
Lacticaseibacillus
Lactobacillus
Ligilactobacillus
Limosilactobacillus
Megasphaera
Prevotella
Rothia
Veillonella
Prevotella_7Prevotella_7

Revision editor(s): Abiola-Salako, Scholastica

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/18

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Fig 2B

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized non-COVID-19 patients versus local controls.

Abundance in Group 1: decreased abundance in Non-Covid-19 Patients

NCBI Quality ControlLinks
Actinobacillus
Alysiella
Aminipila
Bacillus
Bergeyella
Bifidobacterium
Blautia
Candidatus Saccharimonas
Catonella
Enterococcus
Escherichia/Shigella sp.
Faecalibacterium
Gemella
Haemophilus
Lautropia
Lawsonella
Lentimicrobium
Neisseria
Oribacterium
Peptostreptococcus
Ruminococcus
Staphylococcus
Stomatobaculum
Treponema
F0058F0058

Revision editor(s): Abiola-Salako, Scholastica

Experiment 3


Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/18

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
COVID-19 2019 novel coronavirus,2019 novel coronavirus infection,2019-nCoV,2019-nCoV infection,beta-CoV,beta-CoVs,betacoronavirus,coronavirus disease 2019,SARS-coronavirus 2,SARS-CoV-2,severe acute respiratory syndrome coronavirus 2,severe acute respiratory syndrome coronavirus 2 infectious disease,β-coronavirus,β-CoV,β-CoVs,COVID-19,cOVID-19
Group 0 name Corresponds to the control (unexposed) group for case-control studies
non-Covid-19 patients
Group 1 name Corresponds to the case (exposed) group for case-control studies
Covid-19 patients
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Hospitalised Covid-19 patients.
Group 0 sample size Number of subjects in the control (unexposed) group
69
Group 1 sample size Number of subjects in the case (exposed) group
76

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/18

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Fig 2C

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized COVID-19 versus non-COVID-19 patients.

Abundance in Group 1: increased abundance in Covid-19 patients

NCBI Quality ControlLinks
Alloprevotella
Bergeyella
Campylobacter
Candidatus Saccharimonas
Catonella
Enterococcus
Granulicatella
Haemophilus
Lawsonella
Moraxella
Peptostreptococcus
Solobacterium
Candidatus Nanosynbacter lyticus

Revision editor(s): Abiola-Salako, Scholastica

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/18

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Fig 2C

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized COVID-19 versus non-COVID-19 patients.

Abundance in Group 1: decreased abundance in Covid-19 patients

NCBI Quality ControlLinks
Anaeroglobus
Lacticaseibacillus
Lactobacillus
Ligilactobacillus
Limosilactobacillus
Mogibacterium
Rothia

Revision editor(s): Abiola-Salako, Scholastica

Experiment 4


Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/21

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Pneumonia acute pneumonia,chest infection due to pneumonia,pneumonia,Pneumonia (disorder),Pneumonia (disorder) [Ambiguous],Pneumonia due to other specified organism,Pneumonia due to other specified organisms,Pneumonia due to other specified organisms (disorder),Pneumonia NOS,Pneumonia NOS (disorder),pneumonia with infectious disease,Pneumonitis,Pneumonitis (disorder),Pneumonia
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Covid-19 with no Pneumonia
Group 1 name Corresponds to the case (exposed) group for case-control studies
Covid-19 with Pneumonia
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Hospitalized COVID-19 patients with Pneumonia
Group 0 sample size Number of subjects in the control (unexposed) group
38
Group 1 sample size Number of subjects in the case (exposed) group
38

Lab analysis

Statistical Analysis

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/21

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Figure 6A

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized COVID-19 patients with pneumonia compared to those with no pneumonia.

Abundance in Group 1: increased abundance in Covid-19 with Pneumonia

NCBI Quality ControlLinks
Escherichia/Shigella sp.

Revision editor(s): Abiola-Salako, Scholastica

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/21

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Figure 6A

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized COVID-19 patients with pneumonia compared to those with no pneumonia.

Abundance in Group 1: decreased abundance in Covid-19 with Pneumonia

NCBI Quality ControlLinks
Moraxella
Peptoniphilus

Revision editor(s): Abiola-Salako, Scholastica

Experiment 5


Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/21

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Viral load viral burden,viral titer,viral titre,Viral load,viral load
Group 0 name Corresponds to the control (unexposed) group for case-control studies
viral load (≤7.5)
Group 1 name Corresponds to the case (exposed) group for case-control studies
viral load (>7.5)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
COVID-19 patients with viral load greater than 7.5
Group 0 sample size Number of subjects in the control (unexposed) group
33
Group 1 sample size Number of subjects in the case (exposed) group
35

Lab analysis

Statistical Analysis

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/22

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Figure 6B

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized COVID-19 patients with viral load ≤7.5 versus viral load >7.5.

Abundance in Group 1: increased abundance in viral load (>7.5)

NCBI Quality ControlLinks
Acholeplasma
Bacteroides
Porphyromonas
[Eubacterium] nodatum
Family XIII UCG-001Family XIII UCG-001

Revision editor(s): Abiola-Salako, Scholastica

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/22

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Figure 6B

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized COVID-19 patients with viral load ≤7.5 versus viral load >7.5.

Abundance in Group 1: decreased abundance in viral load (>7.5)

NCBI Quality ControlLinks
Enterococcus
Gemella
Paraburkholderia caballeronis
Pseudomonas

Revision editor(s): Abiola-Salako, Scholastica

Experiment 6


Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/22

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
COVID-19 2019 novel coronavirus,2019 novel coronavirus infection,2019-nCoV,2019-nCoV infection,beta-CoV,beta-CoVs,betacoronavirus,coronavirus disease 2019,SARS-coronavirus 2,SARS-CoV-2,severe acute respiratory syndrome coronavirus 2,severe acute respiratory syndrome coronavirus 2 infectious disease,β-coronavirus,β-CoV,β-CoVs,COVID-19,cOVID-19
Group 0 name Corresponds to the control (unexposed) group for case-control studies
local controls
Group 1 name Corresponds to the case (exposed) group for case-control studies
Hospitalized patients
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Hospitalized COVID and non-COVID patients,
Group 0 sample size Number of subjects in the control (unexposed) group
76
Group 1 sample size Number of subjects in the case (exposed) group
145

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Richness Number of species
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/22

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Figure 4A

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized (COVID-19 and non-COVID-19) patients versus local controls.

Abundance in Group 1: increased abundance in Hospitalized patients

NCBI Quality ControlLinks
Actinomyces
Alloprevotella
Atopobium
Centipeda
Ligilactobacillus
Limosilactobacillus
Megasphaera
Prevotella
Solobacterium
Veillonella
Prevotella_7Prevotella_7

Revision editor(s): Abiola-Salako, Scholastica

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2024-7-5

Curated date: 2024/03/22

Curator: Abiola-Salako

Revision editor(s): Abiola-Salako, Scholastica

Source: Figure 4A

Description: Discriminative bacterial genera identified by Linear discriminant analysis (LDA) effect size (LEfSe) in hospitalized (COVID-19 and non-COVID-19) patients versus local controls.

Abundance in Group 1: decreased abundance in Hospitalized patients

NCBI Quality ControlLinks
Actinobacillus
Alysiella
Aminipila
Bacillus
Bacteroides
Bifidobacterium
Blautia
Catonella
Escherichia/Shigella sp.
Faecalibacterium
Finegoldia
Gemella
Haemophilus
Lautropia
Lawsonella
Lentimicrobium
Neisseria
Oribacterium
Ruminococcus
Staphylococcus
Stomatobaculum
Tannerella
Treponema
F0058F0058

Revision editor(s): Abiola-Salako, Scholastica