Population structure of human gut bacteria in a diverse cohort from rural Tanzania and Botswana

doi:10.1186/s13059-018-1616-9

Comparative Study

. 2019 Jan 22;20(1):16.

doi: 10.1186/s13059-018-1616-9.

Population structure of human gut bacteria in a diverse cohort from rural Tanzania and Botswana

Matthew E B Hansen¹, Meagan A Rubel², Aubrey G Bailey^{3

4}, Alessia Ranciaro¹, Simon R Thompson^{1

5}, Michael C Campbell^{1

6}, William Beggs¹, Jaanki R Dave^{1

7}, Gaonyadiwe G Mokone⁸, Sununguko Wata Mpoloka⁹, Thomas Nyambo¹⁰, Christian Abnet¹¹, Stephen J Chanock¹¹, Frederic D Bushman³, Sarah A Tishkoff^{12

13}

Affiliations

¹ Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
² Department of Anthropology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, 19104, USA.
³ Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
⁴ Present address: Kuopio Center for Gene and Cell Therapy, Microkatu 1, 70210, Kuopio, Finland.
⁵ Present address: Genomics England, Queen Mary University of London, London, EC1M 6BQ, UK.
⁶ Present address: Department of Biology, Howard University, 415 College St. NW, Washington, DC, USA.
⁷ The Geisinger Commonwealth Medical College, Scranton, PA, 18509, USA.
⁸ Department of Biomedical Sciences, University of Botswana School of Medicine, Gaborone, Botswana.
⁹ Department of Biological Sciences, University of Botswana, Gaborone, Botswana.
¹⁰ Department of Biochemistry, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania.
¹¹ Cancer Genomics Research Laboratory, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, 20892, USA.
¹² Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA. tishkoff@pennmedicine.upenn.edu.
¹³ Department of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, 19104, USA. tishkoff@pennmedicine.upenn.edu.

PMID: 30665461
PMCID: PMC6341659
DOI: 10.1186/s13059-018-1616-9

Comparative Study

Population structure of human gut bacteria in a diverse cohort from rural Tanzania and Botswana

Matthew E B Hansen et al. Genome Biol. 2019.

. 2019 Jan 22;20(1):16.

doi: 10.1186/s13059-018-1616-9.

Authors

Affiliations

¹ Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
² Department of Anthropology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, 19104, USA.
³ Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA.
⁴ Present address: Kuopio Center for Gene and Cell Therapy, Microkatu 1, 70210, Kuopio, Finland.
⁵ Present address: Genomics England, Queen Mary University of London, London, EC1M 6BQ, UK.
⁶ Present address: Department of Biology, Howard University, 415 College St. NW, Washington, DC, USA.
⁷ The Geisinger Commonwealth Medical College, Scranton, PA, 18509, USA.
⁸ Department of Biomedical Sciences, University of Botswana School of Medicine, Gaborone, Botswana.
⁹ Department of Biological Sciences, University of Botswana, Gaborone, Botswana.
¹⁰ Department of Biochemistry, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania.
¹¹ Cancer Genomics Research Laboratory, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, 20892, USA.
¹² Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA. tishkoff@pennmedicine.upenn.edu.
¹³ Department of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, 19104, USA. tishkoff@pennmedicine.upenn.edu.

PMID: 30665461
PMCID: PMC6341659
DOI: 10.1186/s13059-018-1616-9

Abstract

Background: Gut microbiota from individuals in rural, non-industrialized societies differ from those in individuals from industrialized societies. Here, we use 16S rRNA sequencing to survey the gut bacteria of seven non-industrialized populations from Tanzania and Botswana. These include populations practicing traditional hunter-gatherer, pastoralist, and agropastoralist subsistence lifestyles and a comparative urban cohort from the greater Philadelphia region.

Results: We find that bacterial diversity per individual and within-population phylogenetic dissimilarity differs between Botswanan and Tanzanian populations, with Tanzania generally having higher diversity per individual and lower dissimilarity between individuals. Among subsistence groups, the gut bacteria of hunter-gatherers are phylogenetically distinct from both agropastoralists and pastoralists, but that of agropastoralists and pastoralists were not significantly different from each other. Nearly half of the Bantu-speaking agropastoralists from Botswana have gut bacteria that are very similar to the Philadelphian cohort. Based on imputed metagenomic content, US samples have a relative enrichment of genes found in pathways for degradation of several common industrial pollutants. Within two African populations, we find evidence that bacterial composition correlates with the genetic relatedness between individuals.

Conclusions: Across the cohort, similarity in bacterial presence/absence compositions between people increases with both geographic proximity and genetic relatedness, while abundance weighted bacterial composition varies more significantly with geographic proximity than with genetic relatedness.

Keywords: Adaptation; Agropastoralists; Diet; Genetics; Gut microbiome; Hunter-gatherers; Industrialization; Pastoralists; Rural populations; Sub-Saharan Africa.

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Conflict of interest statement

Ethics approval and consent to participate

All experiments were approved by the University of Pennsylvania Institutional Review Board (IRB # 807981). Ethical approval and permits were also obtained from the following institutions prior to sample collection: The Commission for Science and Technology and National Institute for Medical Research in Dar es Salaam and the Ministry of Health in the Republic of Botswana. Written, informed consent was obtained from each participant.

All experimental methods were in accordance with Helsinki Declaration.

Consent for publication

All participants provided consent for publication of study results of the collected biomaterials paired with anonymized information on age, sex, and location.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

**Fig. 1**
Map of the sampled population groups

**Fig. 2**
The relative abundance per individual for the ten most common taxa, shown for the bacterial taxonomic rank of a Order and b Family. c The population distribution of the relative proportion of *Bacteroidales* per total of *Bacteroidales* and *Clostridiales*

**Fig. 3**
Within group mean α and β diversity. a Shannon index. b Unweighted UniFrac distance distribution within group. c Weighted UniFrac distance distribution within group. The within-population mean Shannon diversity versus unweighted and weighted UniFrac distances are shown in d and e, respectively

**Fig. 4**
PERMANOVA tests of the phylogenetic difference between pairs of groups, based on unweighted UniFrac (panels a, b, c) and weighted UniFrac (panels d, e, f). Shown are groups defined by country of origin (panels a, d), subsistence practice (panels b, e), and sex (panels c, f). The subsistence practices are abbreviated as US = western (Philadelphian), HG = hunter-gatherers (Hadza, San), AP = agropastoralists (Bantu agropastoralists, Burunge, Sandawe), and PA = pastoralists (Herero, Maasai). Bar in red denote pairs where the F-statistic p value is < 0.05

**Fig. 5**
Principle coordinate analysis (PCoA) for weighted UniFrac distances. a The first two principle coordinates for all individuals in the study, where marker shape and color denote the population of origin. Sidebar (panels b and c) show the abundances of *Prevotellaceae* (Prev.), *Bacteroidaceae* (Bact.), and *Ruminococcaceae* (Rumi.) aligned to the first two principal coordinates. d Box-and-whisker distributions between each African population and the US samples, over all pairs of individuals

**Fig. 6**
Box-and-whisker plots of relative abundances distributions per group for the taxa that varied significantly among groups by the ANCOM tests, where individuals are grouped by a traditional or industrial lifestyle, b country of origin, c population, and d traditional subsistence strategy

See this image and copyright information in PMC

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References

1. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Sears MR, et al. Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin Immunol. 2013;9:15. doi: 10.1186/1710-1492-9-15. - DOI - PMC - PubMed
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[1] Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Sears MR, et al. Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin Immunol. 2013;9:15. doi: 10.1186/1710-1492-9-15. - DOI - PMC - PubMed

[2] Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Sears MR, et al. Infant gut microbiota and the hygiene hypothesis of allergic disease: impact of household pets and siblings on microbiota composition and diversity. Allergy Asthma Clin Immunol. 2013;9:15. doi: 10.1186/1710-1492-9-15. - DOI - PMC - PubMed

[3] Blaser M, Bork P, Fraser C, Knight R, Wang J. The microbiome explored: recent insights and future challenges. Nat Rev Microbiol. 2013;11:213–217. doi: 10.1038/nrmicro2973. - DOI - PubMed

[4] Blaser M, Bork P, Fraser C, Knight R, Wang J. The microbiome explored: recent insights and future challenges. Nat Rev Microbiol. 2013;11:213–217. doi: 10.1038/nrmicro2973. - DOI - PubMed

[5] Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, et al. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinforma Oxf Engl. 2012;28:2106–2113. doi: 10.1093/bioinformatics/bts342. - DOI - PMC - PubMed

[6] Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, et al. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinforma Oxf Engl. 2012;28:2106–2113. doi: 10.1093/bioinformatics/bts342. - DOI - PMC - PubMed

[7] Chong CW, Ahmad AF, Lim YAL, Teh CSJ, Yap IKS, Lee SC, et al. Effect of ethnicity and socioeconomic variation to the gut microbiota composition among pre-adolescent in Malaysia. Sci Rep. 2015;5:13338. - PMC - PubMed

[8] Chong CW, Ahmad AF, Lim YAL, Teh CSJ, Yap IKS, Lee SC, et al. Effect of ethnicity and socioeconomic variation to the gut microbiota composition among pre-adolescent in Malaysia. Sci Rep. 2015;5:13338. - PMC - PubMed

[9] Consortium THMP Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–214. doi: 10.1038/nature11234. - DOI - PMC - PubMed

[10] Consortium THMP Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207–214. doi: 10.1038/nature11234. - DOI - PMC - PubMed

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