Different Gut Microbial Profiles in Sub-Saharan African and South Asian Women of Childbearing Age Are Primarily Associated With Dietary Intakes

Minghua Tang, Daniel N Frank, Antoinette Tshefu, Adrien Lokangaka, Shivaprasad S Goudar, Sangappa M Dhaded, Manjunath S Somannavar, Audrey E Hendricks, Diana Ir, Charles E Robertson, Jennifer F Kemp, Rebecca L Lander, Jamie E Westcott, K Michael Hambidge, Nancy F Krebs, Minghua Tang, Daniel N Frank, Antoinette Tshefu, Adrien Lokangaka, Shivaprasad S Goudar, Sangappa M Dhaded, Manjunath S Somannavar, Audrey E Hendricks, Diana Ir, Charles E Robertson, Jennifer F Kemp, Rebecca L Lander, Jamie E Westcott, K Michael Hambidge, Nancy F Krebs

Abstract

Background: To compare and characterize the gut microbiota in women of childbearing age from sub-Saharan Africa (the Democratic Republic of the Congo, DRC) and South Asia (India), in relation to dietary intakes.

Methods: Women of childbearing age were recruited from rural DRC and India as part of the Women First (WF) preconception maternal nutrition trial. Findings presented include fecal 16S rRNA gene-based profiling of women in the WF trial from samples obtained at the time of randomization, prior to initiation of nutrition intervention and to conception.

Results: Stool samples were collected from 217 women (DRC n = 117; India n = 100). Alpha diversity of the gut microbiota was higher in DRC than in India (Chao1: 91 ± 11 vs. 82 ± 12, P = 6.58E-07). The gut microbial community structure was not significantly affected by any demographical or environmental variables, such as maternal BMI, education, and water source. Prevotella, Succinivibrio, and Roseburia were at relatively high abundance without differences between sites. Bifidobacterium was higher in India (4.95 ± 1.0%) than DRC (0.3 ± 0.1%; P = 2.71E-27), as was Lactobacillus (DRC: 0.2 ± 0.0%; India: 1.2 ± 0.1%; P = 2.39E-13) and Faecalibacterium (DRC: 6.0 ± 1.7%; India: 8.4 ± 2.9%; P = 6.51E-7). Ruminococcus was higher in DRC (2.3 ± 0.7%) than in India (1.8 ± 0.4%; P = 3.24E-5) and was positively associated with consumption of flesh foods. Succinivibrio was positively associated with dairy intake in India and fish/insects in DRC. Faecalibacterium was positively associated with vitamin A-rich fruits and vegetables. Overall, these observations were consistent with India being primarily vegetarian with regular fermented dairy consumption and DRC regularly consuming animal-flesh foods.

Conclusion: Consumption of animal-flesh foods and fermented dairy foods were independently associated with the gut microbiota while demographic variables were not, suggesting that diet may have a stronger association with microbiota than demographic characteristics.

Keywords: Democratic Republic of the Congo; India; Women; diet; microbiota.

Figures

FIGURE 1
FIGURE 1
Weighted UniFrac PCoA plots at genus level showing beta diversity of DRC and Indian participants. PERMANOVA F-value: 26.439; R-squared: 0.10951; p-value < 0.001.
FIGURE 2
FIGURE 2
Relative abundance of the gut microbiota phylum between India and DRC. Stacked bar represented percentage abundance. Small taxa with counts less than 150000 were merged as others.
FIGURE 3
FIGURE 3
Relative abundance of the gut microbiota families between India and DRC. Stacked bar represented percentage abundance. Small taxa with counts less than 150000 were merged as others.
FIGURE 4
FIGURE 4
Correlations between dietary intakes and the gut microbiota. Heatmaps summarize Spearman correlation coefficients (rho values) and p-values for pairwise comparisons of dietary intakes and bacterial genera. (A) Correlations of nutrients and bacterial genera in DRC. (B) Correlations of food groups and bacterial genera in DRC. (C) Correlations of nutrients and bacterial genera in India. (D) Correlations of food groups and bacterial genera in India. To simplify visualization, only the 20 most abundant genus-level taxa are presented in these plots. Nominally statistically significant relationships are indicated by overlying symbols: *p < 0.05; +p < 0.01. Dendrograms on the left and top axes of each plot show the results of hierarchical clustering of taxa and nutrients, respectively, based on Euclidean distances.

References

    1. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J. B., Massart S., et al. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. U.S.A. 107 14691–14696. 10.1073/pnas.1005963107
    1. Deschasaux M., Bouter K. E., Prodan A., Levin E., Groen A. K., Herrema H., et al. (2018). Depicting the composition of gut microbiota in a population with varied ethnic origins but shared geography. Nat. Med. 24 1526–1531. 10.1038/s41591-018-0160-1
    1. Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 2194–2200. 10.1093/bioinformatics/btr381
    1. Ewing B., Green P. (1998). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8 186–194. 10.1101/gr.8.3.186
    1. Ewing B., Hillier L., Wendl M. C., Green P. (1998). Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8 175–185. 10.1101/gr.8.3.175
    1. Ferrocino I., Di Cagno R., De Angelis M., Turroni S., Vannini L., Bancalari E., et al. (2015). Fecal microbiota in healthy subjects following omnivore, vegetarian and vegan diets: culturable populations and rRNA DGGE profiling. PLoS One 10:e0128669. 10.1371/journal.pone.0128669
    1. Food and Agricultural Organization of the United Nations (2016). Minimum Dietary Diversity for Women: a Guide for Measurement. Rome: FAO.
    1. Frank D. N. (2009). BARCRAWL and BARTAB: software tools for the design and implementation of barcoded primers for highly multiplexed DNA sequencing. BMC Bioinform. 10:362. 10.1186/1471-2105-10-362
    1. Graf D., Di Cagno R., Fak F., Flint H. J., Nyman M., Saarela M., et al. (2015). Contribution of diet to the composition of the human gut microbiota. Microb. Ecol. Health Dis. 26:26164. 10.3402/mehd.v26.26164
    1. Gupta V. K., Paul S., Dutta C. (2017). Geography, ethnicity or subsistence-specific variations in human microbiome composition and diversity. Front. Microbiol. 8:1162. 10.3389/fmicb.2017.01162
    1. Hambidge K. M., Krebs N. F., Westcott J. E., Garces A., Goudar S. S., Kodkany B. S., et al. (2014). Preconception maternal nutrition: a multi-site randomized controlled trial. BMC Pregnancy Childbirth 14:111. 10.1186/1471-2393-14-111
    1. Hambidge K. M., Westcott J. E., Garces A., Figueroa L., Goudar S. S., Dhaded S. M., et al. (2019). A multicountry randomized controlled trial of comprehensive maternal nutrition supplementation initiated before conception: the Women First trial. Am. J. Clin. Nutr. 109 457–469. 10.1093/ajcn/nqy228
    1. Hara N., Alkanani A. K., Ir D., Robertson C. E., Wagner B. D., Frank D. N., et al. (2012). Prevention of virus-induced type 1 diabetes with antibiotic therapy. J. Immunol. 189 3805–3814. 10.4049/jimmunol.1201257
    1. He Y., Wu W., Zheng H. M., Li P., McDonald D., Sheng H. F., et al. (2018). Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat. Med. 24 1532–1535. 10.1038/s41591-018-0164-x
    1. Heiman M. L., Greenway F. L. (2016). A healthy gastrointestinal microbiome is dependent on dietary diversity. Mol. Metab. 5 317–320. 10.1016/j.molmet.2016.02.005
    1. Homo Sapiens Ucsc Hg19 Human Genome Sequence from iGenome: Illumina (2009). Available at: (accessed August 9, 2014).
    1. Khonsari S., Suganthy M., Burczynska B., Dang V., Choudhury M., Pachenari A. (2016). A comparative study of bifidobacteria in human babies and adults. Biosci. Microbiota Food Health 35 97–103. 10.12938/bmfh.2015-006
    1. Koren O., Goodrich J. K., Cullender T. C., Spor A., Laitinen K., Backhed H. K., et al. (2012). Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150 470–480. 10.1016/j.cell.2012.07.008
    1. Kovatcheva-Datchary P., Nilsson A., Akrami R., Lee Y. S., De Vadder F., Arora T., et al. (2015). Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab. 22 971–982. 10.1016/j.cmet.2015.10.001
    1. Lander R. L., Hambidge K. M., Krebs N. F., Westcott J. E., Garces A., Figueroa L., et al. (2017). Repeat 24-hour recalls and locally developed food composition databases: a feasible method to estimate dietary adequacy in a multi-site preconception maternal nutrition RCT. Food Nutr. Res. 61:1311185. 10.1080/16546628.2017.1311185
    1. Lander R. L., Hambidge K. M., Westcott J. E., Tejeda G., Diba T. S., Mastiholi S. C., et al. (2019). Pregnant women in four low-middle income countries have a high prevalence of inadequate dietary intakes that are improved by dietary diversity. Nutrients 11:E1560. 10.3390/nu11071560
    1. Lane D. J., Pace B., Olsen G. J., Stahl D. A., Sogin M. L., Pace N. R. (1985). Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. U.S.A. 82 6955–6959. 10.1073/pnas.82.20.6955
    1. Langmead B., Salzberg S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 357–359. 10.1038/nmeth.1923
    1. Laursen M. F., Andersen L. B., Michaelsen K. F., Molgaard C., Trolle E., Bahl M. I., et al. (2016). Infant gut microbiota development is driven by transition to family foods independent of maternal obesity. mSphere 1:e00069-15. 10.1128/mSphere.00069-15
    1. Marcobal A., Sonnenburg J. L. (2012). Human milk oligosaccharide consumption by intestinal microbiota. Clin. Microbiol. Infect. 18(Suppl. 4), 12–15. 10.1111/j.1469-0691.2012.03863.x
    1. Markle J. G., Frank D. N., Mortin-Toth S., Robertson C. E., Feazel L. M., Rolle-Kampczyk U., et al. (2013). Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339 1084–1088. 10.1126/science.1233521
    1. Morton E. R., Lynch J., Froment A., Lafosse S., Heyer E., Przeworski M., et al. (2015). Variation in rural african gut microbiota is strongly correlated with colonization by Entamoeba and subsistence. PLoS Genet. 11:e1005658. 10.1371/journal.pgen.1005658
    1. Obregon-Tito A. J., Tito R. Y., Metcalf J., Sankaranarayanan K., Clemente J. C., Ursell L. K., et al. (2015). Subsistence strategies in traditional societies distinguish gut microbiomes. Nat. Commun. 6:6505. 10.1038/ncomms7505
    1. O’Keefe S. J., Chung D., Mahmoud N., Sepulveda A. R., Manafe M., Arch J., et al. (2007). Why do African Americans get more colon cancer than Native Africans? J. Nutr. 137(1 Suppl.), 175S–182S. 10.1093/jn/137.1.175S
    1. Ou J., Carbonero F., Zoetendal E. G., DeLany J. P., Wang M., Newton K., et al. (2013). Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am. J. Clin. Nutr. 98 111–120. 10.3945/ajcn.112.056689
    1. Pruesse E., Peplies J., Glockner F. O. (2012). SINA: accurate high throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28 1823–1829. 10.1093/bioinformatics/bts252
    1. Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41 D590–D596. 10.1093/nar/gks1219
    1. Rasmussen H. S., Holtug K., Mortensen P. B. (1988). Degradation of amino acids to short-chain fatty acids in humans. An in vitro study. Scand. J. Gastroenterol. 23 178–182. 10.3109/00365528809103964
    1. Rehman A., Rausch P., Wang J., Skieceviciene J., Kiudelis G., Bhagalia K., et al. (2016). Geographical patterns of the standing and active human gut microbiome in health and IBD. Gut 65 238–248. 10.1136/gutjnl-2014-308341
    1. Robertson C. E., Harris J. K., Wagner B. D., Granger D., Browne K., Tatem B., et al. (2013). Explicet: graphical user interface software for metadata-driven management, analysis and visualization of microbiome data. Bioinformatics 29 3100–3101. 10.1093/bioinformatics/btt526
    1. Rothschild D., Weissbrod O., Barkan E., Kurilshikov A., Korem T., Zeevi D., et al. (2018). Environment dominates over host genetics in shaping human gut microbiota. Nature 555 210–215. 10.1038/nature25973
    1. Schloss P. D., Westcott S. L. (2011). Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl. Environ. Microbiol. 77 3219–3226. 10.1128/AEM.02810-10
    1. Schnorr S. L., Candela M., Rampelli S., Centanni M., Consolandi C., Basaglia G., et al. (2014). Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 5:3654. 10.1038/ncomms4654
    1. Turnbaugh P. J., Hamady M., Yatsunenko T., Cantarel B. L., Duncan A., Ley R. E., et al. (2009). A core gut microbiome in obese and lean twins. Nature 457 480–484. 10.1038/nature07540
    1. Turnbaugh P. J., Ley R. E., Mahowald M. A., Magrini V., Mardis E. R., Gordon J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 1027–1031.
    1. Vangay P., Johnson A. J., Ward T. L., Al-Ghalith G. A., Shields-Cutler R. R., Hillmann B. M., et al. (2018). US immigration westernizes the human gut microbiome. Cell 175 962.e10–972.e10. 10.1016/j.cell.2018.10.029
    1. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173 697–703. 10.1128/jb.173.2.697-703.1991
    1. Wu G. D., Chen J., Hoffmann C., Bittinger K., Chen Y. Y., Keilbaugh S. A., et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science 334 105–108. 10.1126/science.1208344
    1. Yap G. C., Chee K. K., Hong P. Y., Lay C., Satria C. D., Soenarto Y., et al. (2011). Evaluation of stool microbiota signatures in two cohorts of Asian (Singapore and Indonesia) newborns at risk of atopy. BMC Microbiol. 11:193. 10.1186/1471-2180-11-193
    1. Yatsunenko T., Rey F. E., Manary M. J., Trehan I., Dominguez-Bello M. G., Contreras M., et al. (2012). Human gut microbiome viewed across age and geography. Nature 486 222–227. 10.1038/nature11053
    1. Zhu Y., Lin X., Zhao F., Shi X., Li H., Li Y., et al. (2015). Meat, dairy and plant proteins alter bacterial composition of rat gut bacteria. Sci. Rep. 5:15220. 10.1038/srep15220
    1. Zimmer J., Lange B., Frick J. S., Sauer H., Zimmermann K., Schwiertz A., et al. (2012). A vegan or vegetarian diet substantially alters the human colonic faecal microbiota. Eur. J. Clin. Nutr. 66 53–60. 10.1038/ejcn.2011.141

Source: PubMed

3
订阅