Diet changes due to urbanization in South Africa are linked to microbiome and metabolome signatures of Westernization and colorectal cancer

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Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Ramaboli MC, Ocvirk S, Khan Mirzaei M, Eberhart BL, Valdivia-Garcia M, Metwaly A, Neuhaus K, Barker G, Ru J, Nesengani LT, Mahdi-Joest D, Wilson AS, Joni SK, Layman DC, Zheng J, Mandal R, Chen Q, Perez MR, Fortuin S, Gaunt B, Wishart D, Methé B, Haller D, Li JV, Deng L, Swart R, O'Keefe SJD
Journal
Nature communications
Year
2024
Transition from traditional high-fiber to Western diets in urbanizing communities of Sub-Saharan Africa is associated with increased risk of non-communicable diseases (NCD), exemplified by colorectal cancer (CRC) risk. To investigate how urbanization gives rise to microbial patterns that may be amenable by dietary intervention, we analyzed diet intake, fecal 16 S bacteriome, virome, and metabolome in a cross-sectional study in healthy rural and urban Xhosa people (South Africa). Urban Xhosa individuals had higher intakes of energy (urban: 3,578 ± 455; rural: 2,185 ± 179 kcal/d), fat and animal protein. This was associated with lower fecal bacteriome diversity and a shift from genera favoring degradation of complex carbohydrates (e.g., Prevotella) to taxa previously shown to be associated with bile acid metabolism and CRC. Urban Xhosa individuals had higher fecal levels of deoxycholic acid, shown to be associated with higher CRC risk, but similar short-chain fatty acid concentrations compared with rural individuals. Fecal virome composition was associated with distinct gut bacterial communities across urbanization, characterized by different dominant host bacteria (urban: Bacteriodota; rural: unassigned taxa) and variable correlation with fecal metabolites and dietary nutrients. Food and skin microbiota samples showed compositional differences along the urbanization gradient. Rural-urban dietary transition in South Africa is linked to major changes in the gut microbiome and metabolome. Further studies are needed to prove cause and identify whether restoration of specific components of the traditional diet will arrest the accelerating rise in NCDs in Sub-Saharan Africa.

Experiment 1


Needs review

Curated date: 2024/04/26

Curator: Scholastica

Revision editor(s): Scholastica

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
Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Diet Dietary,Diets,Diet,diet
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Rural Xhosa Cohort
Group 1 name Corresponds to the case (exposed) group for case-control studies
Urban Xhosa Cohort
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
People from Urban Xhosa of South Africa transitioning from traditional high-fiber to Western diets
Group 0 sample size Number of subjects in the control (unexposed) group
21
Group 1 sample size Number of subjects in the case (exposed) group
20
Antibiotics exclusion Number of days without antibiotics usage (if applicable) and other antibiotics-related criteria used to exclude participants (if any)
Oral or I.V antibiotic therapy within the last 6 weeks

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
Not specified
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
3

Alpha Diversity

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

Signature 1

Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Source: Fig. 1D

Description: Significantly differential bacterial genera identified by linear discriminant analysis (LDA) effect size (LEfSe) in fecal samples of Rural Xhosa versus Urban Xhosa cohorts

Abundance in Group 1: increased abundance in Urban Xhosa Cohort

NCBI Quality ControlLinks
Bacteroides
Phascolarctobacterium
Fusobacterium
Butyrivibrio
Mediterraneibacter gnavus
Lachnoclostridium
Thomasclavelia
Alistipes
[Clostridium] innocuum
Bilophila
Flavonifractor
Odoribacter
Barnesiella
CAG_56CAG_56
Oscillibacter
Eisenbergiella
Negativibacillus

Revision editor(s): Scholastica

Signature 2

Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Source: Fig. 1D

Description: Significantly differential bacterial genera identified by linear discriminant analysis (LDA) effect size (LEfSe) in fecal samples of Rural Xhosa versus Urban Xhosa cohorts

Abundance in Group 1: decreased abundance in Urban Xhosa Cohort

NCBI Quality ControlLinks
Oribacterium
UCG_009UCG_009
Candidatus Soleaferrea
Elusimicrobium
uncultured Prevotellaceae bacterium
Prevotellaceae NK3B31 groupPrevotellaceae NK3B31 group
Lachnospiraceae bacterium NK3A20
Selenomonas
Rikenellaceae RC9 gut groupRikenellaceae RC9 gut group
Treponema
Dialister
Faecalibacterium
Prevotella

Revision editor(s): Scholastica

Experiment 2


Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Differences from previous experiment shown

Subjects

Group 0 sample size Number of subjects in the control (unexposed) group
19
Group 1 sample size Number of subjects in the case (exposed) group
9

Lab analysis

Statistical Analysis

Statistical test
ANOVA
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
Not specified

Alpha Diversity

Richness Number of species
unchanged

Signature 1

Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Source: Fig. 3C

Description: Differentially abundant viral contigs (VCs) in rural (n=19) compared to urban (n=9) Xhosa fecal samples

Abundance in Group 1: increased abundance in Urban Xhosa Cohort

NCBI Quality ControlLinks
Faecalibacterium
Muribaculaceae
Prevotella
Bacteroides
Agathobaculum

Revision editor(s): Scholastica

Signature 2

Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Source: Fig. 3C

Description: Differentially abundant viral contigs (VCs) in rural (n=19) compared to urban (n=9) Xhosa fecal samples

Abundance in Group 1: decreased abundance in Urban Xhosa Cohort

NCBI Quality ControlLinks
Oscillospiraceae
Parabacteroides
Bacteroides
Lactococcus
Leuconostoc
Prevotella

Revision editor(s): Scholastica

Experiment 3


Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Differences from previous experiment shown

Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Ingested food Ingested food,ingested food
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Food from rural Xhosa households
Group 1 name Corresponds to the case (exposed) group for case-control studies
Food from urban Xhosa households
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Food samples collected from representative households of urban Xhosa of South Africa
Group 0 sample size Number of subjects in the control (unexposed) group
7
Group 1 sample size Number of subjects in the case (exposed) group
6

Lab analysis

Statistical Analysis

Statistical test
Mann-Whitney (Wilcoxon)

Alpha Diversity

Richness Number of species
decreased

Signature 1

Needs review

Curated date: 2024/04/30

Curator: Idiaru angela

Revision editor(s): Idiaru angela

Source: Figure 4D

Description: Significantly different abundance at the genus level. Statistical analysis using a two-sided Wilcoxon test corrected for multiple testing by the Benjamini–Hochberg method using normalized samples

Abundance in Group 1: decreased abundance in Food from urban Xhosa households

NCBI Quality ControlLinks
Rosenbergiella
Weissella

Revision editor(s): Idiaru angela

Experiment 4


Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Differences from previous experiment shown

Subjects

Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Manual digit skin Digit of hand skin,Digit of terminal segment of free upper limb skin,Digitus manus skin,Finger skin,Fore limb digit skin,Hand digit skin,Skin of digit of hand,Skin of digit of terminal segment of free upper limb,Skin of digitus manus,Skin of finger,Skin of hand digit,Skin of terminal segment of free upper limb digit,Terminal segment of free upper limb digit skin,Manual digit skin,manual digit skin
Group 0 name Corresponds to the control (unexposed) group for case-control studies
Rural Xhosa Cohort
Group 1 name Corresponds to the case (exposed) group for case-control studies
Urban Xhosa Cohort
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Hand skin swabs from urban Xhosa cohort of South Africa

Lab analysis

Statistical Analysis

Alpha Diversity

Richness Number of species
unchanged

Signature 1

Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Source: Supplementary Table 3

Description: Significantly different abundant bacterial genera or families on hand skin swabs from rural versus urban Xhosa cohorts

Abundance in Group 1: increased abundance in Urban Xhosa Cohort

NCBI Quality ControlLinks
Acinetobacter
Aerococcus
Alkanindiges
Aquabacterium
Collinsella
Desemzia
Flaviflexus
Finegoldia
Jeotgalicoccus
Paracoccus
Prevotella
Planomicrobium
Psychrobacter
Ruminococcus
Thermomonas
Trichococcus
Succinivibrio
Vibrio

Revision editor(s): Scholastica

Signature 2

Needs review

Curated date: 2024/04/28

Curator: Scholastica

Revision editor(s): Scholastica

Source: Supplementary Table 3

Description: Significantly different abundant bacterial genera or families on hand skin swabs from rural versus urban Xhosa cohorts

Abundance in Group 1: decreased abundance in Urban Xhosa Cohort

NCBI Quality ControlLinks
Actinomycetospora
Bacillus
Lactococcus
Lysinibacillus
Marmoricola
Methylobacterium-MethylorubrumMethylobacterium-Methylorubrum
Novosphingobium
Ochrobactrum
Peptoniphilus
Peptostreptococcaceae
Serratia
Sphingomonas
Weeksellaceae
Williamsia
Weissella

Revision editor(s): Scholastica