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

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Reviewed Marked as Reviewed by Peace Sandy on 2024-2-10
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
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


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

Curated date: 2023/10/06

Curator: Karen254.

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

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

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

Curated date: 2023/10/09

Curator: Karen254.

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

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

NCBI Quality ControlLinks
Streptococcus pneumoniae
Streptococcus pseudopneumoniae
Streptococcus mitis
Haemophilus influenzae
Fusobacterium nucleatum
Parvimonas micra

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

Signature 2

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

Curated date: 2023/10/09

Curator: Karen254.

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

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 ControlLinks
Haemophilus parahaemolyticus
Neisseria sicca
Anaerococcus
Staphylococcus lugdunensis
Hoylesella buccalis

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

Experiment 2


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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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

NCBI Quality ControlLinks
Bacillus
Prevotella melaninogenica
Veillonella atypica
Burkholderia
Fusobacterium necrophorum

Revision editor(s): Peace Sandy

Signature 2

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Haemophilus parahaemolyticus
Haemophilus sputorum
Corynebacterium propinquum
Lawsonella clevelandensis
Curvibacter gracilis
Dolosigranulum pigrum
Fusobacterium nucleatum
Parvimonas micra
Hoylesella buccalis

Revision editor(s): Peace Sandy

Experiment 3


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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Streptococcus pneumoniae
Streptococcus mitis
Moraxella catarrhalis
Haemophilus influenzae
Fusobacterium nucleatum

Revision editor(s): Peace Sandy

Signature 2

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Staphylococcus lugdunensis
Sphingomonas sp. FARSPH
Dermacoccus nishinomiyaensis

Revision editor(s): Peace Sandy

Experiment 4


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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Streptococcus pneumoniae
Capnocytophaga
Parvimonas micra
Campylobacter showae
Capnocytophaga granulosa
uncultured Lachnospiraceae bacterium
Capnocytophaga sputigena
Tannerella

Revision editor(s): Peace Sandy

Signature 2

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Leptotrichia
Alloprevotella tannerae
uncultured bacterium

Revision editor(s): Peace Sandy

Experiment 5


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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Bacillus
Streptococcus pneumoniae
Burkholderia
Selenomonas sputigena
Haemophilus paraphrohaemolyticus

Revision editor(s): Peace Sandy

Signature 2

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Neisseria
Haemophilus parahaemolyticus
Alloprevotella tannerae
Hoylesella shahii
Campylobacter showae
Tannerella
Treponema
Lautropia dentalis

Revision editor(s): Peace Sandy

Experiment 6


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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Streptococcus pneumoniae
Haemophilus parahaemolyticus
Fusobacterium nucleatum
Rothia mucilaginosa
Aggregatibacter segnis
Haemophilus parainfluenzae
Prevotella melaninogenica
Veillonella
Oribacterium asaccharolyticum

Revision editor(s): Peace Sandy

Signature 2

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

Curated date: 2024/02/10

Curator: Peace Sandy

Revision editor(s): Peace Sandy

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 ControlLinks
Porphyromonas gingivalis
Alloprevotella rava
Prevotella
Prevotella melaninogenica
Neisseria

Revision editor(s): Peace Sandy