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. 2019 Jul 24;14(7):e0215262.
doi: 10.1371/journal.pone.0215262. eCollection 2019.

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

Na Fei  1 , Beatriz Peñalver Bernabé  1 , Louise Lie  2 , Danny Baghdan  2 , Kweku Bedu-Addo  3 , Jacob Plange-Rhule  3 , Terrence E Forrester  4 , Estelle V Lambert  5 , Pascal Bovet  6   7 , Neil Gottel  1 , Walter Riesen  8 , Wolfgang Korte  8 , Amy Luke  2 , Stephanie A Kliethermes  9 , Brian T Layden  10   11 , Jack A Gilbert  1 , Lara R Dugas  2
Affiliations

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

Na Fei et al. PLoS One. .

Abstract

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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Gut bacterial alpha diversity associations with cardiometabolic risk factors (adjusted for age, sex and BMI, only significant associated were shown here).
a) Alpha diversity (Shannon index) in the four study sites (USA, RSA, Ghana and Jamaica); b) association with hypertension in RSA; c); association with elevated fasting blood glucose in Jamaica; d); association with hypertension in Ghana. * p <0.05; ** p <0.01.
Fig 2
Fig 2. Gut bacterial structure and function correlates with cardiometabolic (CM) risk phenotype.
(a), Alpha diversity analysis (Shannon Index) from 16S rRNA gene sequence data of gut microbiota against CM risk; (b-c), Principal coordinate analyses (PCoA) of weighted (a) and unweighted (b) UniFrac distance of gut microbiota composition against CM risk (fdr-corrected p <0.01); (d), Specific gut bacterial taxa are differentially abundant (in relative terms) between study sites with and without elevated CM risk (only significantly differential exact sequence variants (ESVs) with relative abundance ≥ 1% in at least one group shown. Data shown are means ± S.E.M.; p(fdr-corrected) <0.05); (e), Relative abundance of the genes involved in the four different pathways for butyrate synthesis against CM risk of gut microbiota across all study sites. (Data shown are means of percentages ± S.E.M. p(fdr-corrected) < 0.05). CMD means CM risk defined as at least 3 CM risk factors from five: waist circumference, elevated blood pressure, elevated blood fasting glucose, elevated triglyceride and low HDL concentration in USA, RSA, and Ghana *** p < 0.001. false discovery rate.
Fig 3
Fig 3. Oral-associated bacterial structure correlates with CM risk phenotype.
(a-b), Principal coordinate analyses (PCoA) of weighted (a) and unweighted (b) UniFrac distance of oral microbiota composition against CM risk (fdr-corrected p <0.01). (c), Specific oral bacterial taxa are differentially abundant (in relative terms) between study sites with and without CM risk (only significantly differential exact sequence variants (ESVs) with relative abundance ≥ 1% in at least one group shown. Data shown are mean± S.E.M. p(fdr-corrected) < 0.05). CMD means CM risk, including at least 3 CM risk factors of waist circumference, elevated blood pressure, elevated blood fasting glucose, high triglyceridemia and low HDL-cholesterolemia in USA, RSA, and Ghana. fdr, false discovery rate.
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