Gut Microbiome of Coexisting BaAka Pygmies and Bantu Reflects Gradients of Traditional Subsistence Patterns

Cell Reports

Volumn 14, Issue 9, 2016, Pages 2142-2153

  Gomez, Andres ^a,k   Petrzelkova, Klara J ^b,c,d   Burns, Michael B ^a   Yeoman, Carl J ^e   Amato, Katherine R ^f   Vlckova, Klara ^g   Modry, David ^c,g   Todd, Angelique ^h   Jost Robinson, Carolyn A ⁱ   Remis, Melissa J ^j   Torralba, Manolito G ^k   Morton, Elise ^a   Umaña, Juan D ^l   Carbonero, Franck ^m   Gaskins, H Rex ^l   Nelson, Karen E ^k   Wilson, Brenda A ^l   Stumpf, Rebecca M ^l   White, Bryan A ^l   Leigh, Steven R ^l,n   Blekhman, Ran ^a   more..

^a UNIVERSITY OF MINNESOTA   (United States)

^b INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^c INSTITUTE OF PARASITOLOGY   (Czech Republic)

^d Liberec Zoo   (Czech Republic)

^e MONTANA STATE UNIVERSITY   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

^g UNIVERSITY OF VETERINARY AND PHARMACEUTICAL SCIENCES   (Czech Republic)

^h World Wildlife Fund   (Central African Republic)

ⁱ UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^j PURDUE UNIVERSITY   (United States)

^k J CRAIG VENTER INSTITUTE   (United States)

^l UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^m UNIVERSITY OF ARKANSAS   (United States)

ⁿ UNIVERSITY OF COLORADO   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID METABOLISM; ARTICLE; BACTERIAL VIRULENCE; BAKA PYGMY; BANTU PEOPLE; CLOSTRIDIACEAE; CONTROLLED STUDY; ETHNIC DIFFERENCE; FEMALE; FIRMICUTES; HUMAN; INTESTINE FLORA; MALE; METABOLOMICS; NONHUMAN; POPULATION ABUNDANCE; PREVOTELLACEAE; PRIORITY JOURNAL; PYROSEQUENCING; TREPONEMA; VITAMIN METABOLISM; XENOBIOTIC METABOLISM; BACTERIAL GENE; BACTEROIDETES; BLACK PERSON; CENTRAL AFRICAN REPUBLIC; COMPARATIVE STUDY; GENE REGULATORY NETWORK; GENETICS; MOLECULAR TYPING; PALEOLITHIC DIET; SEQUENCE ANALYSIS; UNITED STATES; WESTERN DIET;

BACTERIAL RNA; RNA 16S;

AFRICAN CONTINENTAL ANCESTRY GROUP; BACTEROIDETES; CENTRAL AFRICAN REPUBLIC; DIET, PALEOLITHIC; DIET, WESTERN; FEMALE; FIRMICUTES; GASTROINTESTINAL MICROBIOME; GENE REGULATORY NETWORKS; GENES, BACTERIAL; HUMANS; MALE; MOLECULAR TYPING; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, RNA; UNITED STATES;

EID: 84960468261     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.02.013     Document Type: Article

References (64)

1. Bailey R.C., Head G., Jenike M., Owen B., Rechtman R., Zechenter E. Hunting and gathering in tropical rain forest: is it possible?. Am. Anthropol. 1989, 91:59-82.
2. Blekhman R., Goodrich J.K., Huang K., Sun Q., Bukowski R., Bell J.T., Spector T.D., Keinan A., Ley R.E., Gevers D., Clark A.G. Host genetic variation impacts microbiome composition across human body sites. Genome Biol. 2015, 16:191.
3. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K., Gordon J.I., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7:335-336.
4. Carbonero F., Benefiel A.C., Alizadeh-Ghamsari A.H., Gaskins H.R. Microbial pathways in colonic sulfur metabolism and links with health and disease. Front. Physiol. 2012, 3:448.
5. Cho I., Blaser M.J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 2012, 13:260-270.
6. Cordain L., Eaton S.B., Miller J.B., Mann N., Hill K. The paradoxical nature of hunter-gatherer diets: meat-based, yet non-atherogenic. Eur. J. Clin. Nutr. 2002, 56(Suppl 1):S42-S52.
7. Cordain L., Eaton S.B., Sebastian A., Mann N., Lindeberg S., Watkins B.A., O'Keefe J.H., Brand-Miller J. Origins and evolution of the western diet: health implications for the 21st century. Am. J. Clin. Nutr. 2005, 81:341-354.
8. Daniel H., Moghaddas Gholami A., Berry D., Desmarchelier C., Hahne H., Loh G., Mondot S., Lepage P., Rothballer M., Walker A., et al. High-fat diet alters gut microbiota physiology in mice. ISME J. 2014, 8:295-308.
9. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S., Collini S., Pieraccini G., Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. USA 2010, 107:14691-14696.
10. Dounias E. The management of wild yam tubers by the Baka Pygmies in Southern Cameroon. Afr. Stud. Monogr. 2001, 26(Suppl):135-156.
11. Dudeja P.K., Kode A., Alnounou M., Tyagi S., Torania S., Subramanian V.S., Said H.M. Mechanism of folate transport across the human colonic basolateral membrane. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 281:G54-G60.
12. Dufrene M., Legendre P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 1997, 67:345-366.
13. Flint H.J., Bayer E.A. Plant cell wall breakdown by anaerobic microorganisms from the Mammalian digestive tract. Ann. N Y Acad. Sci. 2008, 1125:280-288.
14. Flint H.J., Bayer E.A., Rincon M.T., Lamed R., White B.A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 2008, 6:121-131.
15. Gasparic A., Marinsek-Logar R., Martin J., Wallace R.J., Nekrep F.V., Flint H.J. Isolation of genes encoding β-D-xylanase, β-D-xylosidase and α-L-arabinofuranosidase activities from the rumen bacterium Prevotella ruminicola B1(4). FEMS Microbiol. Lett. 1995, 125:135-141.
16. Giraudoux P. pgirmess: data analysis in ecology 2014, Department of Chrono-Environment, University of Franche-Comté.
17. Gomez A., Petrzelkova K., Yeoman C.J., Vlckova K., Mrázek J., Koppova I., Carbonero F., Ulanov A., Modry D., Todd A., et al. Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Mol. Ecol. 2015, 24:2551-2565.
18. Gomez A., Rothman J.M., Petrzelkova K., Yeoman C.J., Vlckova K., Umana J.D., Carr M., Modry D., Todd A., Torralba M., et al. Temporal variation selects for diet-microbe co-metabolic traits in the gut of Gorilla spp. ISME J. 2016, 146:514-526. Published online August 28, 2015. 10.1038/ismej.2015.146.
19. Goodrich J.K., Waters J.L., Poole A.C., Sutter J.L., Koren O., Blekhman R., Beaumont M., Van Treuren W., Knight R., Bell J.T., et al. Human genetics shape the gut microbiome. Cell 2014, 159:789-799.
20. Haiser H.J., Turnbaugh P.J. Developing a metagenomic view of xenobiotic metabolism. Pharmacol. Res. 2013, 69:21-31.
21. Han C., Gronow S., Teshima H., Lapidus A., Nolan M., Lucas S., Hammon N., Deshpande S., Cheng J.F., Zeytun A., et al. Complete genome sequence of Treponema succinifaciens type strain (6091). Stand. Genomic Sci. 2011, 4:361-370.
22. Hart T.B., Hart J.A. The ecological basis of hunter-gatherer subsistence in African rain forests: the Mbuti of Eastern Zaire. Hum. Ecol. 1986, 14:29-55.
23. Hasegawa H., Modrý D., Kitagawa M., Shutt K.A., Todd A., Kalousová B., Profousová I., Petrželková K.J. Humans and great apes cohabiting the forest ecosystem in Central African Republic harbour the same hookworms. PLoS Negl. Trop. Dis. 2014, 8:e2715.
24. Hewlett B.S. Hunter-Gatherers of the Congo Basin: Cultures, Histories, and Biology of African Pygmies 2014, Transaction Publishers.
25. Structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214. Human Microbiome Project Consortium.
26. Hume I. Fermentation in the hindgut of mammals. Gastrointestinal Microbiology. Volumne 1. Gastrointesinal Ecosystems and Fermentations 1997, 84-115. Chapman & Hall. R.I. Mackie, B.A. White (Eds.).
27. Isong E., Adewusi S., Nkanga E., Umoh E., Offiong E. Nutritional and phytogeriatological studies of three varieties of Gnetum africanum ('afang'). Food Chem. 1999, 64:489-493.
28. Jarvis J.P., Scheinfeldt L.B., Soi S., Lambert C., Omberg L., Ferwerda B., Froment A., Bodo J.M., Beggs W., Hoffman G., et al. Patterns of ancestry, signatures of natural selection, and genetic association with stature in Western African pygmies. PLoS Genet. 2012, 8:e1002641.
29. Langille M.G.I., Zaneveld J., Caporaso J.G., McDonald D., Knights D., Reyes J.A., Clemente J.C., Burkepile D.E., Vega Thurber R.L., Knight R., et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 2013, 31:814-821.
30. Ley R.E., Turnbaugh P.J., Klein S., Gordon J.I. Microbial ecology: human gut microbes associated with obesity. Nature 2006, 444:1022-1023.
31. Lin A., Bik E.M., Costello E.K., Dethlefsen L., Haque R., Relman D.A., Singh U. Distinct distal gut microbiome diversity and composition in healthy children from Bangladesh and the United States. PLoS ONE 2013, 8:e53838.
32. Louis P., Hold G.L., Flint H.J. The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 2014, 12:661-672.
33. Manzel A., Muller D.N., Hafler D.A., Erdman S.E., Linker R.A., Kleinewietfeld M. Role of "western diet" in inflammatory autoimmune diseases. Curr. Allergy Asthma Rep. 2014, 14:404.
34. Martínez I., Stegen J.C., Maldonado-Gómez M.X., Eren A.M., Siba P.M., Greenhill A.R., Walter J. The gut microbiota of rural papua new guineans: composition, diversity patterns, and ecological processes. Cell Rep. 2015, 11:527-538.
35. Migliano A.B., Vinicius L., Lahr M.M. Life history trade-offs explain the evolution of human pygmies. Proc. Natl. Acad. Sci. USA 2007, 104:20216-20219.
36. Moeller A.H., Li Y., Mpoudi Ngole E., Ahuka-Mundeke S., Lonsdorf E.V., Pusey A.E., Peeters M., Hahn B.H., Ochman H. Rapid changes in the gut microbiome during human evolution. Proc. Natl. Acad. Sci. USA 2014, 111:16431-16435.
37. Morton E.R., Lynch J., Froment A., Lafosse S., Heyer E., Przeworski M., Blekhman R., Ségurel L. Variation in rural African gut microbiota is strongly correlated with colonization by entamoeba and subsistence. PLoS Genet. 2015, 11:e1005658.
38. Mukhopadhya I., Hansen R., Nicholl C.E., Alhaidan Y.A., Thomson J.M., Berry S.H., Pattinson C., Stead D.A., Russell R.K., El-Omar E.M., Hold G.L. A comprehensive evaluation of colonic mucosal isolates of Sutterella wadsworthensis from inflammatory bowel disease. PLoS ONE 2011, 6:e27076.
39. Myles I.A., Fontecilla N.M., Janelsins B.M., Vithayathil P.J., Segre J.A., Datta S.K. Parental dietary fat intake alters offspring microbiome and immunity. J. Immunolo. 2013, 191:3200-3209.
40. Nenadic O., Greenacre M. Correspondence analysis in R, with two- and three-dimensional graphics: the ca package. J. Stat. Softw. 2007, 20:1-13.
41. O'Keefe S.J.D., Li J.V., Lahti L., Ou J., Carbonero F., Mohammed K., Posma J.M., Kinross J., Wahl E., Ruder E., et al. Fat, fibre and cancer risk in African Americans and rural Africans. Nat. Commun. 2015, 6:6342.
42. Obregon-Tito A.J., Tito R.Y., Metcalf J., Sankaranarayanan K., Clemente J.C., Ursell L.K., Zech Xu Z., Van Treuren W., Knight R., Gaffney P.M., et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat. Commun. 2015, 6:6505.
43. Oksanen, J., Guillaume Blanchet, F., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H., and Wagner, H. (2012.) vegan: community ecology package.
44. Ou J., Carbonero F., Zoetendal E.G., DeLany J.P., Wang M., Newton K., Gaskins H.R., O'Keefe S.J. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am. J. Clin. Nutr. 2013, 98:111-120.
45. Perry G.H., Foll M., Grenier J.C., Patin E., Nédélec Y., Pacis A., Barakatt M., Gravel S., Zhou X., Nsobya S.L., et al. Adaptive, convergent origins of the pygmy phenotype in African rainforest hunter-gatherers. Proc. Natl. Acad. Sci. USA 2014, 111:E3596-E3603.
46. R: a language and environment for statistical computing 2014, R Development Core Team, R Foundation for Statistical Computing.
47. Remis M.J., Jost Robinson C.A. Examining short-term nutritional status among BaAka foragers in transitional economies. Am. J. Phys. Anthropol. 2014, 154:365-375.
48. Revelle W. psych: procedures for psychological, psychometric, and personality research 2014, Northwestern University.
49. Roberts, D.W. (2012.) labsdv: ordination and multivariate analysis for ecology.
50. Schnorr S.L., Candela M., Rampelli S., Centanni M., Consolandi C., Basaglia G., Turroni S., Biagi E., Peano C., Severgnini M., et al. Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 2014, 5:3654.
51. Schwager, E., et al. (In progress, February 8, 2016.) Detecting statistically significant associations between sparse and high dimensional compositional data.
52. Sekimoto H., Shimada O., Makanishi M., Nakano T., Katayama O. Interrelationship between serum and fecal sterols. Jpn. J. Med. 1983, 22:14-20.
53. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
54. Sousa T., Paterson R., Moore V., Carlsson A., Abrahamsson B., Basit A.W. The gastrointestinal microbiota as a site for the biotransformation of drugs. Int. J. Pharm. 2008, 363:1-25.
55. Tito R.Y., Knights D., Metcalf J., Obregon-Tito A.J., Cleeland L., Najar F., Roe B., Reinhard K., Sobolik K., Belknap S., et al. Insights from characterizing extinct human gut microbiomes. PLoS ONE 2012, 7:e51146.
56. Turnbaugh P.J., Ley R.E., Mahowald M.A., Magrini V., Mardis E.R., Gordon J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444:1027-1031.
57. Ulijaszek S.J., Lofink H. Obesity in biocultural perspective. Annu. Rev. Anthropol. 2006, 35:337-360.
58. Van den Abbeele P., Van de Wiele T., Verstraete W., Possemiers S. The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiol. Rev. 2011, 35:681-704.
59. Vendeville A., Winzer K., Heurlier K., Tang C.M., Hardie K.R. Making 'sense' of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 2005, 3:383-396.
60. Windey K., De Preter V., Verbeke K. Relevance of protein fermentation to gut health. Mol. Nutr. Food Res. 2012, 56:184-196.
61. Yamauchi T., Sato H., Kawamura K. Nutritional status, activity pattern, and dietary intake among the Baka hunter-gatherers in the village camps in Cameroon. Afr. Study Monogr. 2000, 21:67-82.
62. Yamauchi T., Sato H., Kawamura K. Nutritional status and physical fitness of Pygmy hunter-gatherers living in the African rainforests. Afr. Stud. Monogr. 2014, 47(Suppl):25-34.
63. Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Magris M., Hidalgo G., Baldassano R.N., Anokhin A.P., et al. Human gut microbiome viewed across age and geography. Nature 2012, 486:222-227.
64. Zhang X., Wu C., Wu H., Sheng L., Su Y., Zhang X., Luan H., Sun G., Sun X., Tian Y., et al. Anti-hyperlipidemic effects and potential mechanisms of action of the caffeoylquinic acid-rich Pandanus tectorius fruit extract in hamsters fed a high fat-diet. PLoS ONE 2013, 8:e61922.