The upper respiratory tract microbiota of healthy adults is affected by Streptococcus pneumoniae carriage, smoking habits, and contact with children

Study information

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

study design

case-control

Citation

PMID PubMed identifier for scientific articles.

37658443

DOI Digital object identifier for electronic documents.

https://doi.org/10.1186/s40168-023-01640-9

URI

Authors

Paulo AC, Lança J, Almeida ST, Hilty M, Sá-Leão R

Journal

Microbiome

Year

2023

Keywords:

Healthy adults, Microbiota, Nasopharynx, Oropharynx, Streptococcus pneumoniae

BACKGROUND: The microbiota of the upper respiratory tract is increasingly recognized as a gatekeeper of respiratory health. Despite this, the microbiota of healthy adults remains understudied. To address this gap, we investigated the composition of the nasopharyngeal and oropharyngeal microbiota of healthy adults, focusing on the effect of Streptococcus pneumoniae carriage, smoking habits, and contact with children. RESULTS: Differential abundance analysis indicated that the microbiota of the oropharynx was significantly different from that of the nasopharynx (P < 0.001) and highly discriminated by a balance between the classes Negativicutes and Bacilli (AUC of 0.979). Moreover, the oropharynx was associated with a more homogeneous microbiota across individuals, with just two vs. five clusters identified in the nasopharynx. We observed a shift in the nasopharyngeal microbiota of carriers vs. noncarriers with an increased relative abundance of Streptococcus, which summed up to 30% vs. 10% in noncarriers and was not mirrored in the oropharynx. The oropharyngeal microbiota of smokers had a lower diversity than the microbiota of nonsmokers, while no differences were observed in the nasopharyngeal microbiota. In particular, the microbiota of smokers, compared with nonsmokers, was enriched (on average 16-fold) in potential pathogenic taxa involved in periodontal diseases of the genera Bacillus and Burkholderia previously identified in metagenomic studies of cigarettes. The microbiota of adults with contact with children resembled the microbiota of children. Specifically, the nasopharyngeal microbiota of these adults had, on average, an eightfold increase in relative abundance in Streptococcus sp., Moraxella catarrhalis, and Haemophilus influenzae, pathobionts known to colonize the children's upper respiratory tract, and a fourfold decrease in Staphylococcus aureus and Staphylococcus lugdunensis. CONCLUSIONS: Our study showed that, in adults, the presence of S. pneumoniae in the nasopharynx is associated with a shift in the microbiota and dominance of the Streptococcus genus. Furthermore, we observed that smoking habits are associated with an increase in bacterial genera commonly linked to periodontal diseases. Interestingly, our research also revealed that adults who have regular contact with children have a microbiota enriched in pathobionts frequently carried by children. These findings collectively contribute to a deeper understanding of how various factors influence the upper respiratory tract microbiota in adults. Video Abstract.

Experiment 1

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

Curated date: 2023/10/06

Curator: Karen254.

Revision editor(s): WikiWorks, Chloe, Peace Sandy, Karen254.

Subjects

Location of subjects

Portugal

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

Nasopharyngeal gland , Saliva Nasopharyngeal gland,nasopharyngeal gland,Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology

Streptococcus pneumoniae Diplococcus pneumoniae,Micrococcus pneumoniae,Streptococcus pneumoniae,streptococcus pneumoniae

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Pneumococcal non-carriers.

Group 1 name Corresponds to the case (exposed) group for case-control studies

Pneumococcal carriers

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Individuals who carry pneumococci in the nasopharynx

Group 0 sample size Number of subjects in the control (unexposed) group

47

Group 1 sample size Number of subjects in the case (exposed) group

12

Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)

1 month

Lab analysis

Sequencing type

16S

16S variable region One or more hypervariable region(s) of the bacterial 16S gene

V4

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance

MGISEQ-2000

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).

relative abundances

Statistical test

Mann-Whitney (Wilcoxon)

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

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

decreased

Richness Number of species

decreased

Signature 1

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

Curated date: 2023/10/09

Curator: Karen254.

Revision editor(s): WikiWorks, Chloe, Peace Sandy, Karen254.

Source: Table S2.

Description: Bacteria (ASV) differentially present in the nasopharyngeal microbiota of pneumococcal carriers and non-carriers.

Abundance in Group 1: increased abundance in Pneumococcal carriers

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Streptococcus pneumoniae
Streptococcus pseudopneumoniae
Streptococcus mitis
Haemophilus influenzae
Fusobacterium nucleatum
Parvimonas micra

Revision editor(s): WikiWorks, Chloe, Peace Sandy, Karen254.

Signature 2

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Curated date: 2023/10/09

Curator: Karen254.

Revision editor(s): WikiWorks, Chloe, Peace Sandy, Karen254.

Source: Table S2

Description: Bacteria (ASV) differentially present in the nasopharyngeal microbiota of pneumococcal carriers and non-carriers.

Abundance in Group 1: decreased abundance in Pneumococcal carriers

NCBI	Quality Control	Links
Haemophilus parahaemolyticus
Neisseria sicca
Anaerococcus
Staphylococcus lugdunensis
Hoylesella buccalis

Revision editor(s): WikiWorks, Chloe, Peace Sandy, Karen254.

Experiment 2

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

Curated date: 2024/02/10

Curator: Peace Sandy

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

non- smokers

Group 1 name Corresponds to the case (exposed) group for case-control studies

Smokers

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

The nasopharyngeal area of smokers

Group 0 sample size Number of subjects in the control (unexposed) group

20

Group 1 sample size Number of subjects in the case (exposed) group

5

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

unchanged

Simpson Estimator of species richness and species evenness: more weight on species evenness

unchanged

Richness Number of species

unchanged

Signature 1

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Source: Table S3

Description: Bacteria (ASV) differentially present in the nasopharyngeal microbiota of smokers and non-smokers.

Abundance in Group 1: increased abundance in Smokers

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Bacillus
Prevotella melaninogenica
Veillonella atypica
Burkholderia
Fusobacterium necrophorum

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Signature 2

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Source: Table S3

Description: Bacteria (ASV) differentially present in the nasopharyngeal microbiota of smokers and non-smokers

Abundance in Group 1: decreased abundance in Smokers

NCBI	Quality Control	Links
Haemophilus parahaemolyticus
Haemophilus sputorum
Corynebacterium propinquum
Lawsonella clevelandensis
Curvibacter gracilis
Dolosigranulum pigrum
Fusobacterium nucleatum
Parvimonas micra
Hoylesella buccalis

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Experiment 3

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Curated date: 2024/02/10

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

No contact with children

Group 1 name Corresponds to the case (exposed) group for case-control studies

Contact with children

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

The nasopharyngeal microbiota of individuals that regular contact with children.

Group 0 sample size Number of subjects in the control (unexposed) group

22

Group 1 sample size Number of subjects in the case (exposed) group

10

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

unchanged

Simpson Estimator of species richness and species evenness: more weight on species evenness

unchanged

Inverse Simpson Modification of Simpsons index D as 1/D to obtain high values in datasets of high diversity and vice versa

unchanged

Signature 1

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Source: Table S4

Description: Bacteria (ASV) differentially present in the nasopharyngeal microbiota of individuals that have and do not have regular contact with children.

Abundance in Group 1: increased abundance in Contact with children

NCBI	Quality Control	Links
Streptococcus pneumoniae
Streptococcus mitis
Moraxella catarrhalis
Haemophilus influenzae
Fusobacterium nucleatum

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Signature 2

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

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Source: Table S4

Description: Bacteria (ASV) differentially present in the nasopharyngeal microbiota of individuals that have and do not have regular contact with children.

Abundance in Group 1: decreased abundance in Contact with children

NCBI	Quality Control	Links
Staphylococcus lugdunensis
Sphingomonas sp. FARSPH
Dermacoccus nishinomiyaensis

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Experiment 4

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

Curated date: 2024/02/10

Curator: Peace Sandy

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Differences from previous experiment shown

Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology

Oropharyngeal gland , Saliva Gland of oral part of pharynx,Gland of oropharynx,Oral part of pharynx gland,Oropharynx gland,Oropharyngeal gland,oropharyngeal gland,Sailva normalis,Saliva atomaris,Saliva molecularis,Salivary gland secretion,Saliva,saliva

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Pneumococcal non-carriers.

Group 1 name Corresponds to the case (exposed) group for case-control studies

Pneumococcal carriers

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Oropharyngeal microbiota of pneumococcal carriers

Group 0 sample size Number of subjects in the control (unexposed) group

47

Group 1 sample size Number of subjects in the case (exposed) group

12

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

decreased

Simpson Estimator of species richness and species evenness: more weight on species evenness

decreased

Richness Number of species

decreased

Signature 1

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Source: Table S5

Description: Bacteria (ASV) differentially present in the oropharyngeal microbiota of pneumococcal carriers and non-carriers.

Abundance in Group 1: increased abundance in Pneumococcal carriers

NCBI	Quality Control	Links
Streptococcus pneumoniae
Capnocytophaga
Parvimonas micra
Campylobacter showae
Capnocytophaga granulosa
uncultured Lachnospiraceae bacterium
Capnocytophaga sputigena
Tannerella

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Signature 2

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Source: Table S5

Description: Bacteria (ASV) differentially present in the oropharyngeal microbiota of pneumococcal carriers and non-carriers.

Abundance in Group 1: decreased abundance in Pneumococcal carriers

NCBI	Quality Control	Links
Leptotrichia
Alloprevotella tannerae
uncultured bacterium

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Experiment 5

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

Curated date: 2024/02/10

Curator: Peace Sandy

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

Non- smokers

Group 1 name Corresponds to the case (exposed) group for case-control studies

Smokers

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Oropharyngeal microbiota of smokers

Group 0 sample size Number of subjects in the control (unexposed) group

20

Group 1 sample size Number of subjects in the case (exposed) group

5

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

unchanged

Simpson Estimator of species richness and species evenness: more weight on species evenness

unchanged

Richness Number of species

unchanged

Signature 1

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Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy, WikiWorks

Source: Table S6

Description: Bacteria (ASV) differentially present in the oropharyngeal microbiota of smokers and non-smokers.

Abundance in Group 1: increased abundance in Smokers

NCBI	Quality Control	Links
Bacillus
Streptococcus pneumoniae
Burkholderia
Selenomonas sputigena
Haemophilus paraphrohaemolyticus

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Signature 2

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Source: Table S6

Description: Bacteria (ASV) differentially present in the oropharyngeal microbiota of smokers and non-smokers.

Abundance in Group 1: decreased abundance in Smokers

NCBI	Quality Control	Links
Neisseria
Haemophilus parahaemolyticus
Alloprevotella tannerae
Hoylesella shahii
Campylobacter showae
Tannerella
Treponema
Lautropia dentalis

Revision editor(s): Peace Sandy, WikiWorks

Experiment 6

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

Curated date: 2024/02/10

Curator: Peace Sandy

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Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies

No Contact with Children

Group 1 name Corresponds to the case (exposed) group for case-control studies

Contact with children

Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group

Oropharyngeal microbiota of individuals that have regular contact with children.

Group 0 sample size Number of subjects in the control (unexposed) group

22

Group 1 sample size Number of subjects in the case (exposed) group

10

Lab analysis

Statistical Analysis

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness

unchanged

Simpson Estimator of species richness and species evenness: more weight on species evenness

unchanged

Richness Number of species

unchanged

Signature 1

EditHistoryDelete

Flag for review

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy, WikiWorks

Source: Table S7

Description: Bacteria (ASV) differentially present in the oropharyngeal microbiota of individuals that have and do not have regular contact with children.

Abundance in Group 1: increased abundance in Contact with children

NCBI	Quality Control	Links
Streptococcus pneumoniae
Haemophilus parahaemolyticus
Fusobacterium nucleatum
Rothia mucilaginosa
Aggregatibacter segnis
Haemophilus parainfluenzae
Prevotella melaninogenica
Veillonella
Oribacterium asaccharolyticum

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Signature 2

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Source: Table S7

Description: Bacteria (ASV) differentially present in the oropharyngeal microbiota of individuals that have and do not have regular contact with children

Abundance in Group 1: decreased abundance in Contact with children

NCBI	Quality Control	Links
Porphyromonas gingivalis
Alloprevotella rava
Prevotella
Prevotella melaninogenica
Neisseria

Revision editor(s): Peace Sandy, WikiWorks