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

M. C. Ramaboli, S. Ocvirk, M. Khan Mirzaei, B. L. Eberhart, M. Valdivia-Garcia, A. Metwaly, K. Neuhaus, G. Barker, J. Ru, L. T. Nesengani, D. Mahdi-Joest, A. S. Wilson, S. K. Joni, D. C. Layman, J. Zheng, R. Mandal, Q. Chen, M. R. Perez, S. Fortuin, B. Gaunt, D. Wishart, B. Methé, D. Haller, J. V. Li, L. Deng, R. Swart and S. J. D. O’Keefe ()
Additional contact information
M. C. Ramaboli: Stellenbosch University
S. Ocvirk: University of Pittsburgh
M. Khan Mirzaei: Institute of Virology, Helmholtz Centre Munich - German Research Centre for Environmental Health
B. L. Eberhart: University of Pittsburgh
M. Valdivia-Garcia: Faculty of Medicine, Imperial College London
A. Metwaly: Technical University of Munich
K. Neuhaus: Technical University of Munich
G. Barker: Faculty of Medicine, Imperial College London
J. Ru: Institute of Virology, Helmholtz Centre Munich - German Research Centre for Environmental Health
L. T. Nesengani: University of South Africa
D. Mahdi-Joest: German Institute of Human Nutrition
A. S. Wilson: University of Pittsburgh
S. K. Joni: University of the Western Cape
D. C. Layman: University of the Western Cape
J. Zheng: University of Alberta
R. Mandal: University of Alberta
Q. Chen: Faculty of Medicine, Imperial College London
M. R. Perez: University of Pittsburgh
S. Fortuin: Stellenbosch University
B. Gaunt: Zithulele Hospital
D. Wishart: University of Alberta
B. Methé: University of Pittsburgh
D. Haller: Technical University of Munich
J. V. Li: Faculty of Medicine, Imperial College London
L. Deng: Institute of Virology, Helmholtz Centre Munich - German Research Centre for Environmental Health
R. Swart: University of the Western Cape
S. J. D. O’Keefe: Stellenbosch University

Nature Communications, 2024, vol. 15, issue 1, 1-12

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41467-024-46265-0

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