The microbiome in urogenital schistosomiasis and induced bladder pathologies

Study information

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study design

case-control

Citation

PMID PubMed identifier for scientific articles.

28793309

DOI Digital object identifier for electronic documents.

https://doi.org/10.1371/journal.pntd.0005826

URI

Authors

Adebayo AS, Suryavanshi MV, Bhute S, Agunloye AM, Isokpehi RD, Anumudu CI, Shouche YS

Journal

PLoS neglected tropical diseases

Year

2017

BACKGROUND: Human schistosomiasis is a highly prevalent neglected tropical disease (NTD) caused by Schistosoma species. Research on the molecular mechanisms influencing the outcomes of bladder infection by Schistosoma haematobium is urgently needed to develop new diagnostics, therapeutics and infection prevention strategies. The objective of the research study was to determine the microbiome features and changes in urine during urogenital schistosomiasis and induced bladder pathologies. METHODOLOGY: Seventy participants from Eggua, southwestern Nigeria provided morning urine samples and were screened for urogenital schistosomiasis infection and bladder pathologies in a cross-sectional study. Highthroughput NGS sequencing was carried out, targeting the 16S V3 region. Filtered reads were processed and analyzed in a bioinformatics pipeline. PRINCIPAL FINDINGS: The study participants (36 males and 34 females, between ages 15 and 65) were categorized into four groups according to status of schistosomiasis infection and bladder pathology. Data analytics of the next-generation sequencing reads revealed that Proteobacteria and Firmicutes dominated and had influence on microbiome structure of both non-infected persons and persons with urogenital schistosomiasis. Furthermore, gender and age influenced taxa abundance independent of infection or bladder pathology. Several taxa distinguished urogenital schistosomiasis induced bladder pathologies from urogenital schistosomiasis infection alone and from healthy persons, including known immune-stimulatory taxa such as Fusobacterium, Sphingobacterium and Enterococcus. Some of these significant taxa, especially Sphingobacterium were projected as markers of infection, while several genera including potentially beneficial taxa such as Trabulsiella and Weissella, were markers of the non-infected. Finally, expected changes in protein functional categories were observed to relate to cellular maintenance and lipid metabolism. CONCLUSION: The urinary microbiome is a factor to be considered in developing biomarkers, diagnostic tools, and new treatment for urogenital schistosomiasis and induced bladder pathologies.

Experiment 1

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Curated date: 2024/04/24

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Subjects

Location of subjects

Nigeria

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

Urine Urine,urine

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

Urinary schistosomiasis bladder Schistosomiasis,bladder schistosomiasis,cystitis with bilharziasis,cystitis with bilharziasis (disorder),Schistosoma haematobium,Schistosoma haematobium (& vesical schistosomiasis),Schistosoma haematobium infection,Schistosoma Hematobium Infection,Schistosoma hematobium infection,Schistosoma hematobium infection (disorder),Schistosoma hematobium infectious disease,Schistosomiasis due to schistosoma haematobium,schistosomiasis due to Schistosoma haematobium,Schistosomiasis haematobia,schistosomiasis of bladder,Schistosomiasis of bladder [Ambiguous],urinary bladder schistosomiasis,urinary schistosomiasis,urinary schistosomiasis (disorder),vesical schistosomiasis,Vesical schistosomiasis NOS,Urinary schistosomiasis

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

Healthy Control

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

Infection-Only

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

Urine samples infected with urogenital schistosomiasis

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

13

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

25

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

Recent use of Antibiotics

Lab analysis

Sequencing type

16S

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

V3

Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance

Ion Torrent

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

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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Curated date: 2024/04/25

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Source: Figure 6B

Description: Differentially abundant microbiome between urogenital schistosomiasis (infection-only) and healthy controls

Abundance in Group 1: increased abundance in Infection-Only

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Acinetobacter
Aerococcus
Chryseobacterium
Facklamia
Klebsiella
Pseudomonas
Shewanella
Staphylococcus
unclassified Carnobacteriaceae
unclassified Planococcaceae
unclassified Pseudomonadaceae

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Signature 2

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Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Source: Figure 6B

Description: Differentially abundant microbiome between urogenital schistosomiasis (infection-only) and healthy controls

Abundance in Group 1: decreased abundance in Infection-Only

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Acinetobacter
Edwardsiella
Enterobacter
Erwinia
Gardnerella
Hafnia
Limnobacter
Mycoplana
Photorhabdus
Psychrobacter
Weissella
unclassified Aeromonadales
unclassified Bifidobacteriaceae
unclassified Enterobacteriaceae
unclassified Moraxellaceae
unclassified Pseudomonadaceae
Staphylococcus

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Experiment 2

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Curated date: 2024/04/25

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Differences from previous experiment shown

Subjects

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

Advanced

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

Urine samples infected with urogenital schistosomiasis induced bladder pathology.

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

22

Lab analysis

Statistical Analysis

Alpha Diversity

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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Curated date: 2024/04/29

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Source: Figure 6A

Description: Differentially abundant microbiome between urogenital schistosomiasis induced bladder pathology (advanced) and healthy controls.

Abundance in Group 1: increased abundance in Advanced

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Bacteroides
Jeotgalicoccus
Prevotella
Fusobacterium
Veillonella
Aerococcus
Granulicatella
Facklamia
Brevibacterium
Peptoniphilus
Caulobacter
Lactobacillus
Staphylococcus
Acinetobacter
unclassified Cardiobacteriales

Revision editor(s): Adenike Oladimeji-Kasumu

Signature 2

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Curated date: 2024/04/29

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Source: Figure 6A

Description: Differentially abundant microbiome between urogenital schistosomiasis induced bladder pathology (advanced) and healthy controls.

Abundance in Group 1: decreased abundance in Advanced

NCBI	Quality Control	Links
unclassified Enterococcaceae
unclassified Bifidobacteriaceae
unclassified Pseudoalteromonadaceae
unclassified Enterobacteriaceae
unclassified Moraxellaceae
unclassified Aeromonadales
Enterobacter
Edwardsiella
Weissella
Erwinia
Photorhabdus
Hafnia
Pseudomonas
Staphylococcus
Acinetobacter

Revision editor(s): Adenike Oladimeji-Kasumu

Experiment 3

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Curated date: 2024/04/29

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Differences from previous experiment shown

Subjects

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

Non-Infected

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

Infected

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

Infected with urogenital schistosomiasis

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

24

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

46

Lab analysis

Statistical Analysis

Alpha Diversity

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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Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Source: Figure 5A, 5B

Description: Differentially abundant microbiome genera in urogenital schistosomiasis (infected) and controls (non-infected).

Abundance in Group 1: increased abundance in Infected

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Acinetobacter
Aerococcaceae
Aerococcus
Bacteroidaceae
Bacteroides
Brevibacteriaceae
Brevibacterium
Carnobacteriaceae
Chryseobacterium
Enterococcaceae
Enterococcus
Facklamia
Fusobacteriaceae
Fusobacterium
Granulicatella
Jeotgalicoccus
Lactobacillaceae
Lactobacillus
Lactococcus
Melissococcus
Moraxellaceae
Peptoniphilus
Prevotella
Prevotellaceae
Staphylococcaceae
Staphylococcus
Streptococcaceae
Tissierellaceae
Veillonella
Veillonellaceae
Weeksellaceae
unclassified Cardiobacteriales
unclassified Carnobacteriaceae

Revision editor(s): Adenike Oladimeji-Kasumu

Signature 2

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Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Source: Figure 5A, 5B

Description: Differentially abundant microbiome genera in urogenital schistosomiasis (infected) and controls (non-infected).

Abundance in Group 1: decreased abundance in Infected

NCBI	Quality Control	Links
Acinetobacter
Bacillaceae
Bacillus
Bifidobacteriaceae
Caulobacteraceae
Chryseobacterium
Edwardsiella
Enhydrobacter
Enterobacter
Enterobacteriaceae
Erwinia
Gardnerella
Hafnia
Janthinobacterium
Limnobacter
Moraxellaceae
Mycoplana
Oxalobacteraceae
Photorhabdus
Pseudoalteromonadaceae
Psychrobacter
Staphylococcaceae
Staphylococcus
Weeksellaceae
Weissella
unclassified Aeromonadales
unclassified Bifidobacteriaceae
unclassified Pseudoalteromonadaceae
Lactobacillaceae
Comamonadaceae
unclassified Moraxellaceae
unclassified Enterobacteriaceae

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Experiment 4

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Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Differences from previous experiment shown

Subjects

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

Pathology only

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

Advanced

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

Urogenital schistosomiasis induced bladder pathology.

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

10

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

22

Lab analysis

Statistical Analysis

Alpha Diversity

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

EditHistoryDelete

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-4

Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Source: Figure 5D

Description: Differentially abundant microbiome genera in non-infected bladder pathology (pathology-only) and urogenital schistosomiasis induced bladder pathology (advanced).

Abundance in Group 1: increased abundance in Advanced

NCBI	Quality Control	Links
Acinetobacter
Aerococcus
Bacteroides
Brevibacterium
Comamonas
Facklamia
Fusobacterium
Granulicatella
Jeotgalicoccus
Lactobacillus
Peptoniphilus
Prevotella
Sphingobacterium
Veillonella
Wautersiella
Weeksella
unclassified Cardiobacteriales
unclassified Pseudomonadaceae
Hylemonella

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Signature 2

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Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Source: Figure 5D

Description: Differentially abundant microbiome genera in non-infected bladder pathology (pathology-only) and urogenital schistosomiasis induced bladder pathology (advanced).

Abundance in Group 1: decreased abundance in Advanced

NCBI	Quality Control	Links
Acinetobacter
Bacillus
Chryseobacterium
Edwardsiella
Enhydrobacter
Hafnia
Janthinobacterium
Pseudomonas
Staphylococcus
unclassified Aeromonadales
unclassified Enterobacteriaceae
unclassified Planococcaceae
unclassified Pseudoalteromonadaceae
Erwinia
Photorhabdus

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Experiment 5

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Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Differences from previous experiment shown

Subjects

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

Infection Only

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

urogenital schistosomiasis induced bladder pathology.

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

25

Lab analysis

Statistical Analysis

Alpha Diversity

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

EditHistoryDelete

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-4

Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Source: Figure 5C

Description: Differential microbiome genera between urogenital schistosomiasis (infection-only) and urogenital schistosomiasis induced bladder pathology (advanced).

Abundance in Group 1: increased abundance in Advanced

NCBI	Quality Control	Links
unclassified Pseudomonadaceae
Bacteroides
Prevotella
Jeotgalicoccus
unclassified Moraxellaceae
unclassified Cardiobacteriales
Psychrobacter
Fusobacterium
Veillonella
Granulicatella
Facklamia
Brevibacterium
Peptoniphilus
unclassified Bifidobacteriaceae
Caulobacter
Gardnerella
Sphingobacterium
Wautersiella
Limnobacter
Weeksella
Lactobacillus
Mycoplana
Acinetobacter
Staphylococcus

Revision editor(s): Adenike Oladimeji-Kasumu

Signature 2

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Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Source: Figure 5C

Description: Differential microbiome genera between urogenital schistosomiasis (infection-only) and urogenital schistosomiasis induced bladder pathology (advanced).

Abundance in Group 1: decreased abundance in Advanced

NCBI	Quality Control	Links
unclassified Enterococcaceae
unclassified Carnobacteriaceae
Chryseobacterium
Acinetobacter
Staphylococcus
Pseudomonas
unclassified Planococcaceae

Revision editor(s): Adenike Oladimeji-Kasumu

Experiment 6

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Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Differences from previous experiment shown

Subjects

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

Pathology Only

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

Infection Only

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

Urogenital schistosomiasis infection

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

10

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

25

Lab analysis

Statistical Analysis

Alpha Diversity

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

EditHistoryDelete

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Reviewed Marked as Reviewed by Svetlana up on 2024-6-4

Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Source: Figure S2B

Description: Differential abundance in the urine microbiome of persons with urogenital schistosomiasis infection without bladder pathology (infection-only) and pathology without schistosomiasis infection (pathology-only).

Abundance in Group 1: increased abundance in Infection Only

NCBI	Quality Control	Links
Aerococcus
unclassified Pseudomonadaceae
Comamonas
Enterococcus
Chryseobacterium
Acinetobacter

Revision editor(s): Adenike Oladimeji-Kasumu

Signature 2

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Curated date: 2024/04/30

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu

Source: Figure S2B

Description: Differential abundance in the urine microbiome of persons with urogenital schistosomiasis infection without bladder pathology (infection-only) and pathology without schistosomiasis infection (pathology-only).

Abundance in Group 1: decreased abundance in Infection Only

NCBI	Quality Control	Links
unclassified Pseudoalteromonadaceae
Enterobacter
Edwardsiella
Erwinia
Photorhabdus
Caulobacter
unclassified Enterobacteriaceae
Staphylococcus
Enhydrobacter
Chryseobacterium
Bacillus
Janthinobacterium
Psychrobacter
unclassified Moraxellaceae
Acinetobacter

Revision editor(s): Adenike Oladimeji-Kasumu

Experiment 7

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Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Differences from previous experiment shown

Subjects

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

Non-Infected

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

Infected

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

Not infected with urogenital schistosomiasis.

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

24

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

46

Lab analysis

Statistical Analysis

Statistical test

LEfSe

Alpha Diversity

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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Curated date: 2024/05/01

Curator: Adenike Oladimeji-Kasumu

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Source: Figure 7

Description: Predicted microbial biomarkers in urogenital schistosomiasis cases (infected) and controls (non-infected).

Abundance in Group 1: decreased abundance in Infected

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Anaerococcus
Peptostreptococcaceae
Peptostreptococcus
Streptomycetaceae
Trabulsiella
Weissella
Xenorhabdus
unclassified Enterobacteriaceae
Lactobacillaceae

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Signature 2

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Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica

Source: Figure 7

Description: Predicted microbial biomarkers in urogenital schistosomiasis cases (infected) and controls (non-infected).

Abundance in Group 1: increased abundance in Infected

NCBI	Quality Control	Links
Sphingobacteriaceae
Sphingobacteriales
Sphingobacteriia
Sphingobacterium
Stenotrophomonas
unclassified Bacillales

Revision editor(s): Adenike Oladimeji-Kasumu, Scholastica