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The human microbiota is associated with cardiometabolic risk across the epidemiologic transition

journal contribution
posted on 20.07.2022, 17:49 authored by Na Fei, Beatriz Peñalver Bernabé, Louise Lie, Danny Baghdan, Kweku Bedu-Addo, Jacob Plange-Rhule, Terrence E Forrester, Estelle V Lambert, Pascal Bovet, Neil Gottel, Walter Riesen, Wolfgang Korte, Amy Luke, Stephanie A Kliethermes, Brian LaydenBrian Layden, Jack A Gilbert, Lara R Dugas
Oral and fecal microbial biomarkers have previously been associated with cardiometabolic (CM) risk, however, no comprehensive attempt has been made to explore this association in minority populations or across different geographic regions. We characterized gut- and oral-associated microbiota and CM risk in 655 participants of African-origin, aged 25-45, from Ghana, South Africa, Jamaica, and the United States (US). CM risk was classified using the CM risk cut-points for elevated waist circumference, elevated blood pressure and elevated fasted blood glucose, low high-density lipoprotein (HDL), and elevated triglycerides. Gut-associated bacterial alpha diversity negatively correlated with elevated blood pressure and elevated fasted blood glucose. Similarly, gut bacterial beta diversity was also significantly differentiated by waist circumference, blood pressure, triglyceridemia and HDL-cholesterolemia. Notably, differences in inter- and intra-personal gut microbial diversity were geographic-region specific. Participants meeting the cut-points for 3 out of the 5 CM risk factors were significantly more enriched with Lachnospiraceae, and were significantly depleted of Clostridiaceae, Peptostreptococcaceae, and Prevotella. The predicted relative proportions of the genes involved in the pathways for lipopolysaccharides (LPS) and butyrate synthesis were also significantly differentiated by the CM risk phenotype, whereby genes involved in the butyrate synthesis via lysine, glutarate and 4-aminobutyrate/succinate pathways and LPS synthesis pathway were enriched in participants with greater CM risk. Furthermore, inter-individual oral microbiota diversity was also significantly associated with the CM risk factors, and oral-associated Streptococcus, Prevotella, and Veillonella were enriched in participants with 3 out of the 5 CM risk factors. We demonstrate that in a diverse cohort of African-origin adults, CM risk is significantly associated with reduced microbial diversity, and the enrichment of specific bacterial taxa and predicted functional traits in both gut and oral environments. As well as providing new insights into the associations between the gut and oral microbiota and CM risk, this study also highlights the potential for novel therapeutic discoveries which target the oral and gut microbiota in CM risk.

Funding

The Function and Regulation of the Novel Pregnancy-Specific Hexokinase HKDC1 | Funder: National Institutes of Health (National Institute of Diabetes and Digestive and Kidney Diseases) | Grant ID: R01DK104927

Role of Nutrient Sensing Receptors for the Gut Microbiota in Metabolism | Funder: United States Department of Veterans Affairs | Grant ID: I01BX003382

Arnol O. Beckman Postdoctoral Award | Funder: Arnold and Mabel Beckman Foundation

History

Citation

Fei, N., Bernabé, B. P., Lie, L., Baghdan, D., Bedu-Addo, K., Plange-Rhule, J., Forrester, T. E., Lambert, E. V., Bovet, P., Gottel, N., Riesen, W., Korte, W., Luke, A., Kliethermes, S. A., Layden, B. T., Gilbert, J. A.Dugas, L. R. (2019). The human microbiota is associated with cardiometabolic risk across the epidemiologic transition. PLOS ONE, 14(7), e0215262-. https://doi.org/10.1371/journal.pone.0215262

Publisher

Public Library of Science (PLoS)

Language

en

issn

1932-6203