Gut microbiome of the Hadza hunter-gatherers

ARTICLE Received 22 Nov 2013 | Accepted 14 Mar 2014 | Published 15 Apr 2014 DOI: 10.1038/ncomms4654 OPEN Gut microbiome of the Hadza hunter-gatherers Stephanie L. Schnorr1,*, Marco Candela2,*, Simone Rampelli2, Manuela Centanni2, Clarissa Consolandi3, Giulia Basaglia2, Silvia Turroni2, Elena Biagi2, Clelia Peano3, Marco Severgnini3, Jessica Fiori2, Roberto Gotti2, Gianluca De Bellis3, Donata Luiselli4, Patrizia Brigidi2, Audax Mabulla5, Frank Marlowe6, Amanda G. Henry1 & Alyssa N. Crittenden7 Human gut microbiota directly influences health and provides an extra means of adaptive potential to different lifestyles. To explore variation in gut microbiota and to understand how these bacteria may have co-evolved with humans, here we investigate the phylogenetic diversity and metabolite production of the gut microbiota from a community of human hunter-gatherers, the Hadza of Tanzania. We show that the Hadza have higher levels of microbial richness and biodiversity than Italian urban controls. Further comparisons with two rural farming African groups illustrate other features unique to Hadza that can be linked to a foraging lifestyle. These include absence of Bifidobacterium and differences in microbial composition between the sexes that probably reflect sexual division of labour. Furthermore, enrichment in Prevotella, Treponema and unclassified Bacteroidetes, as well as a peculiar arrangement of Clostridiales taxa, may enhance the Hadza’s ability to digest and extract valuable nutrition from fibrous plant foods. 1 Plant Foods in Hominin Dietary Ecology Research Group, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany. 2 Department of Pharmacy and Biotechnology, University of Bologna, Via Belmeloro 6, 40126 Bologna, Italy. 3 Institute of Biomedical Technologies, Italian National Research Council, Via Fratelli Cervi 93, 20090 Segrate, Milan, Italy. 4 Department of Biological, Geological and Environmental Sciences, University of Bologna, Via Selmi 3, Bologna 40126, Italy. 5 College of Arts and Social Sciences, University of Dar es Salaam, 35091 Dar es Salaam, Tanzania. 6 Division of Biological Anthropology, University of Cambridge, Cambridge CB2 1TN, UK. 7 Metabolism, Anthropometry, and Nutrition Laboratory, Department of Anthropology, University of Nevada, Las Vegas, Nevada 89154-5003, USA. * These authors contributed equally to the work. Correspondence and requests for materials should be addressed to A.G.H. (email: ). NATURE COMMUNICATIONS | 5:3654 | DOI: 10.1038/ncomms4654 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms4654 T he human gut microbiota (GM) is vital for host nutrition, metabolism, pathogen resistance and immune function1, and varies with diet, lifestyle and environment2–4. Together, the host and microbiome have been termed a ‘supraorganism’ whose combined activities represent both a shared target for natural selection and a driver of adaptive responses5. By studying GM variation across human populations, we are able to explore the limits of our genetic and metabolic potential, and the extent to which GM-host co-evolution is responsible for our physiological flexibility and environmental adaptation6–8. Comparative studies between unindustrialized rural communities from Africa and South America and industrialized western communities from Europe and North America have revealed specific GM adaptations to their respective lifestyles. These adaptations include higher biodiversity and enrichment of Bacteroidetes and Actinobacteria in rural communities, and an overall reduction in microbial diversity and stability in western populations4,9. Unindustrialized small-scale rural societies are targets for understanding trends in human–GM interactions because they rely less on antibiotics and sterile cleaners, and often consume a greater breadth of unrefined seasonally available foods10. Yet, despite recent focus on rural societies, there remains a significant gap in our knowledge of the microbe–host relationship among hunter-gatherer populations. This is especially problematic because humans have relied on hunting and gathering for 95% of our evolutionary history. Here, to explore how a foraging subsistence strategy influences GM profiles, we analyse faecal microbiota from 27 Hadza huntergatherers from two separate camp sites (Fig. 1). The Hadza who chose to participate in this study came from the Dedauko and Sengele camps, situated in the Rift Valley ecosystem around the shores of Lake Eyasi in northwestern Tanzania. These participants are part of the B200–300 traditionally living Hadza, who are one of the last remaining hunting and gathering communities in the world. The Hadza live in small mobile camps with fluid membership, usually comprising a core group of B30 people, and target native wild foods, both hunted and foraged, for the bulk of their subsistence11. While the Hadza are a modern human population, they live in a key geographic region for studies of human evolution and target resources similar to those exploited by our hominin ancestors. The Hadza lifestyle therefore is thought to most closely resemble that of Paleolithic humans. We compare phylogenetic diversity, taxonomic relative abundance and the short-chain fatty-acid (SCFA) profile of the Hadza microbiome with those of 16 urban living Italian adults from Bologna, Italy. We then compare these data with previously published data on two different rural African groups from Burkina Faso (BF) and Malawi4,9 to identify GM features unique to the Hadza lifestyle. This study presents the first characterization of a forager GM through work with the Hadza hunter-gatherers, and will allow us to understand how the human microbiota aligns with a foraging lifestyle, one in which all human ancestors participated before the Neolithic transition. Results Dietary information for sampled cohorts. The Hadza diet consists of wild foods that fall into five main categories: meat, honey, baobab, berries and tubers (Supplementary Table 1 and Supplementary Fig. 1)12–14. They practice no cultivation or domestication of plants and animals and receive minimal amounts of agricultural products (o5% of calories) from external sources15. By comparison, the diet of the Italian cohort derives almost entirely from commercial agricultural products and adheres largely to the Mediterranean diet: abundant plant foods, fresh fruit, pasta, bread and olive oil; low-to-moderate 2 amounts of dairy, poultry, fish and red meat (Supplementary Table 2). In addition, the majority of carbohydrates (based on gram amount) came from easily digestible starch (54%) and sugar (36%) while very little was derived from fibre-soluble or -insoluble (10%; Supplementary Fig. 2). Characterization of Hadza microbiota. Faecal samples from 27 Hadza, aged 8–70 years, mean age 32 years and 16 Italians aged 20–40 years, mean age also 3 (...truncated)