The penile microbiota of Black South African men: relationship with human papillomavirus and HIV infection

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Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Onywera H, Williamson AL, Cozzuto L, Bonnin S, Mbulawa ZZA, Coetzee D, Ponomarenko J, Meiring TL
Journal
BMC microbiology
Year
2020
Keywords:
HIV, Human papillomavirus (HPV), Microbiota, Penile
BACKGROUND: To date, the microbiota of the human penis has been studied mostly in connection with circumcision, HIV risk and female partner bacterial vaginosis (BV). These studies have shown that male circumcision reduces penile anaerobic bacteria, that greater abundance of penile anaerobic bacteria is correlated with increased cytokine levels and greater risk of HIV infection, and that the penile microbiota is an important harbour for BV-associated bacteria. While circumcision has been shown to significantly reduce the risk of acquiring human papillomavirus (HPV) infection, the relationship of the penile microbiota with HPV is still unknown. In this study, we examined the penile microbiota of HPV-infected men as well as the impact of HIV status. RESULTS: The penile skin microbiota of 238 men from Cape Town (South Africa) were profiled using Illumina sequencing of the V3-V4 hypervariable regions of the 16S rRNA gene. Corynebacterium and Prevotella were found to be the most abundant genera. Six distinct community state types (CSTs) were identified. CST-1, dominated by Corynebacterium, corresponded to less infections with high-risk HPV (HR-HPV) relative to CSTs 2-6. Men in CST-5 had greater relative abundances of Prevotella, Clostridiales, and Porphyromonas and a lower relative abundance of Corynebacterium. Moreover, they were significantly more likely to have HPV or HR-HPV infections than men in CST-1. Using a machine learning approach, we identified greater relative abundances of the anaerobic BV-associated bacteria (Prevotella, Peptinophilus, and Dialister) and lower relative abundance of Corynebacterium in HR-HPV-infected men compared to HR-HPV-uninfected men. No association was observed between HIV and CST, although the penile microbiota of HIV-infected men had greater relative abundances of Staphylococcus compared to HIV-uninfected men. CONCLUSIONS: We found significant differences in the penile microbiota composition of men with and without HPV and HIV infections. HIV and HR-HPV infections were strongly associated with greater relative abundances of Staphylococcus and BV-associated bacterial taxa (notably Prevotella, Peptinophilus and Dialister), respectively. It is possible that these taxa could increase susceptibility to HIV and HR-HPV acquisition, in addition to creating conditions in which infections persist. Further longitudinal studies are required to establish causal relationships and to determine the extent of the effect.

Experiment 1


Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Subjects

Location of subjects
South Africa
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
Skin of penis Penile skin,Penis skin,Penis zone of skin,Zone of skin of penis,Skin of penis,skin of penis
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Human papillomavirus Human Papilloma Virus,human papillomavirus HPV,Human papillomavirus,human papillomavirus
Group 0 name Corresponds to the control (unexposed) group for case-control studies
High-Risk HPV Negative (HR-HPV Negative)
Group 1 name Corresponds to the case (exposed) group for case-control studies
High-Risk HPV Positive (HR-HPV Positive)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
High-Risk HPV Positive (HR-HPV Positive) refers to individuals infected with Human Papillomavirus.
Group 0 sample size Number of subjects in the control (unexposed) group
81
Group 1 sample size Number of subjects in the case (exposed) group
102

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)
0.2
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
3

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
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

Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Fig. 5

Description: Significant differentially abundant taxa between HR-HPV positive and negative individuals.

Abundance in Group 1: increased abundance in High-Risk HPV Positive (HR-HPV Positive)

NCBI Quality ControlLinks
Peptoniphilus
Dialister
unclassified Eubacteriales
Prevotella

Revision editor(s): KateRasheed

Signature 2

Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Fig. 5

Description: Significant differentially abundant taxa between HR-HPV positive and negative individuals.

Abundance in Group 1: decreased abundance in High-Risk HPV Positive (HR-HPV Positive)

NCBI Quality ControlLinks
Brevibacteriaceae
Actinomycetales

Revision editor(s): KateRasheed

Experiment 2


Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
HR-HPV-uninfected in HIV-negative
Group 1 name Corresponds to the case (exposed) group for case-control studies
HR-HPV-infected in HIV-negative
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
HR-HPV-infected in HIV-negative refers to the presence of High-Risk Human papillomavirus (HPV) in men that are not infected with HIV.
Group 0 sample size Number of subjects in the control (unexposed) group
Not specified
Group 1 sample size Number of subjects in the case (exposed) group
Not specified

Lab analysis

Statistical Analysis

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
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

Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Additional file 5: Figure S3

Description: Significant differentially abundant taxa between HR-HPV-infected in HIV-negative and HR-HPV-uninfected in HIV-negative individuals.

Abundance in Group 1: decreased abundance in HR-HPV-infected in HIV-negative

NCBI Quality ControlLinks
Actinomycetales
Brevibacterium
Brachybacterium

Revision editor(s): KateRasheed

Experiment 3


Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Human immunodeficiency virus AIDS virus,HIV,Human immunodeficiency virus,human immunodeficiency virus
Group 0 name Corresponds to the control (unexposed) group for case-control studies
HIV - negative
Group 1 name Corresponds to the case (exposed) group for case-control studies
HIV - positive
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
HIV - positive refers to individuals infected with Human Immunodeficiency Virus.
Group 0 sample size Number of subjects in the control (unexposed) group
150
Group 1 sample size Number of subjects in the case (exposed) group
88

Lab analysis

Statistical Analysis

LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

Pielou Quantifies how equal the community is numerically
unchanged
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

Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Fig. 6

Description: Significant differentially abundant taxa between HIV positive and negative individuals.

Abundance in Group 1: decreased abundance in HIV - positive

NCBI Quality ControlLinks
unclassified Actinomycetales

Revision editor(s): KateRasheed

Experiment 4


Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Differences from previous experiment shown

Subjects

Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Human papillomavirus Human Papilloma Virus,human papillomavirus HPV,Human papillomavirus,human papillomavirus
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Non-Corynebacterium-dominated microbiota (Diverse penile microbiota (CSTs 2-5))
Group 1 name Corresponds to the case (exposed) group for case-control studies
Corynebacterium-dominated penile microbiota (CST-1)
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Corynebacterium-dominated penile microbiota (CST-1) refers to men who had less HR-HPV.
Group 0 sample size Number of subjects in the control (unexposed) group
111
Group 1 sample size Number of subjects in the case (exposed) group
127

Lab analysis

Statistical Analysis

Alpha Diversity

Pielou Quantifies how equal the community is numerically
decreased
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
Inverse Simpson Modification of Simpsons index D as 1/D to obtain high values in datasets of high diversity and vice versa
decreased

Signature 1

Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Additional file 3: Table S2

Description: Differentially abundant taxa in men with Corynebacterium-dominated versus diverse penile microbiota.

Abundance in Group 1: increased abundance in Corynebacterium-dominated penile microbiota (CST-1)

NCBI Quality ControlLinks
Anaerococcus
Bifidobacterium
Blautia
Brachybacterium
Brevibacterium
Clostridium
Corynebacterium
Delftia
Dermabacter
Enhydrobacter
Eremococcus
Exiguobacterium
Facklamia
Gemmiger
Jeotgalicoccus
Lachnospiraceae incertae sedis
Massilia
Methylobacterium
Neisseria
Propionibacterium
Pseudoclavibacter
Psychrobacter
Roseburia
Salinicoccus
Sphingomonas
Staphylococcus
Tessaracoccus
unclassified Actinomycetales
unclassified Bacillales
unclassified Bacilli
unclassified Bacteria
unclassified Dermabacteraceae
unclassified Neisseriaceae
unclassified Nocardiaceae
unclassified Oxalobacteraceae
unclassified Planococcaceae
unclassified Sphingomonadaceae
unclassified Staphylococcaceae
Nosocomiicoccus
GpGp

Revision editor(s): KateRasheed

Signature 2

Needs review

Curated date: 2024/11/04

Curator: KateRasheed

Revision editor(s): KateRasheed

Source: Additional file 3: Table S2

Description: Differentially abundant taxa in men with Corynebacterium-dominated versus diverse penile microbiota.

Abundance in Group 1: decreased abundance in Corynebacterium-dominated penile microbiota (CST-1)

NCBI Quality ControlLinks
Aeromonas
Arcanobacterium
Atopobium
Bacteroides
Brucella
Campylobacter
Citrobacter
Dialister
Finegoldia
Gardnerella
Granulicatella
Haemophilus
Hallella
Howardella
Kocuria
Micrococcus
Mobiluncus
Murdochiella
Mycoplasma
Negativicoccus
Olsenella
Parvimonas
Peptococcus
Porphyromonas
Prevotella
Pseudomonas
Pyramidobacter
Saccharofermentans
Sneathia
Streptococcus
Sutterella
Tissierellia incertae sedis
Varibaculum
unclassified Aerococcaceae
unclassified Bacillota
unclassified Bacteroidales
unclassified Bacteroidota
unclassified Coriobacteriaceae
unclassified Eubacteriales
unclassified Micrococcaceae
unclassified Peptostreptococcaceae
unclassified Porphyromonadaceae
unclassified Prevotellaceae
unclassified Veillonellaceae
unclassified Incertae Sedis XIunclassified Incertae Sedis XI
unclassified Brucellaceae

Revision editor(s): KateRasheed