Short- and long-read metagenomics of urban and rural South African gut microbiomes reveal a transitional composition and undescribed taxa

Fiona B Tamburini ,Dylan G Maghini ,Stuart A Ali ,Jean-Tristan Brandenburg ,Michaella Hulley ,Shane A Norris ,Dhriti Sengupta ,Theo Mathema ,Alisha N Wade ,Vukosi Baloyi ,Francesc Xavier Gómez‐Olivé ,Herman Sorgho ,Gershim Asiki ,Tinashe Chikowore ,Scott Hazelhurst ,Michèle Ramsay ,Marianne Alberts ,Catherine Kyobutungi ,Cassandra C Soo ,Yaniv Swiel ,Stephen Tollman ,Daniel Ohene-Kwofie ,Ananyo Choudhury ,Given Mashaba ,Ovokeraye H Oduaran ,Floidy Wafawanaka ,Solomon Choma ,Freedom Mukomana ,Ryan G Wagner ,Natalie Smyth ,Godfred Agongo ,Osman Sankoh ,Furahini Tluway ,Ryan Brewster ,Palwendé Romuald Boua ,Christopher Khayeka–Wandabwa ,Engelbert A Nonterah ,Rhian Twine ,Felistas Mashinya ,Ernest Tambo ,Kathleen Kahn ,Venesa Sahibdeen ,Pauline Tindana ,Abraham Oduro ,Himla Soodyall ,Francisco Ceballos ,Nigel J Crowther ,Isaac Kisiangani ,Chodziwadziwa Whiteson Kabudula ,Cornelius Debpuur ,Mwawi Gondwe ,Busisiwe Mthembu ,Henry Wandera ,Halidou Tinto ,Lisa K Micklesfield ,Shukri F Mohamed ,Ami S Bhatt

doi:10.1038/s41467-021-27917-x

Abstract

Human gut microbiome research focuses on populations living in high-income countries and to a lesser extent, non-urban agriculturalist and hunter-gatherer societies. The scarcity of research between these extremes limits our understanding of how the gut microbiota relates to health and disease in the majority of the world’s population. Here, we evaluate gut microbiome composition in transitioning South African populations using short- and long-read sequencing. We analyze stool from adult females living in rural Bushbuckridge (n = 118) or urban Soweto (n = 51) and find that these microbiomes are taxonomically intermediate between those of individuals living in high-income countries and traditional communities. We demonstrate that reference collections are incomplete for characterizing microbiomes of individuals living outside high-income countries, yielding artificially low beta diversity measurements, and generate complete genomes of undescribed taxa, including Treponema, Lentisphaerae, and Succinatimonas. Our results suggest that the gut microbiome of South Africans does not conform to a simple “western-nonwestern” axis and contains undescribed microbial diversity.

Highlights

Human gut microbiome research focuses on populations living in high-income countries and to a lesser extent, non-urban agriculturalist and hunter-gatherer societies
We find that gut microbiome composition differs demonstrably between the Bushbuckridge and Soweto cohorts, further highlighting the importance of studying diverse communities with differing lifestyle practices
This furthers recent work which revealed that crAssphage is prevalent across many cohorts globally[49], but found relatively fewer crAssphage sequences on the African continent, presumably due to paucity of available shotgun metagenomic data

Summary

Introduction

Human gut microbiome research focuses on populations living in high-income countries and to a lesser extent, non-urban agriculturalist and hunter-gatherer societies. A smaller number of studies have characterized the gut microbiome composition of individuals practicing traditional lifestyles[3,4], including communities in Venezuela and Malawi[5], hunter-gatherer communities in Tanzania[6,7,8,9], nonindustrialized populations in Tanzania and Botswana[10], and agriculturalists in Peru[11] and remote Madagascar[12] These cohorts are not representative of how most of the world lives either. Many of the world’s communities lead lifestyles between the extremes of an urbanized, industrialized and relatively high-income lifestyle and traditional subsistence practices It is a scientific and ethical imperative to include these diverse populations in biomedical research, yet dismayingly many of these intermediate groups are underrepresented in or absent from the published microbiome literature. Eight of these studies described the bacterial microbiome[6,7,12,24,25,26,27,28], while one exclusively described the viral metagenome[29]

Methods

Results

Conclusion