The Prevotella copri Complex Comprises Four Distinct Clades Underrepresented in Westernized Populations

Adrian Tett; Kun D Huang; Francesco Asnicar; Hannah Fehlner-Peach; Edoardo Pasolli; Nicolai Karcher; Federica Armanini; Paolo Manghi; Kevin Bonham; Moreno Zolfo; Francesca De Filippis; Cara Magnabosco; Richard Bonneau; John Lusingu; John Amuasi; Karl Reinhard; Thomas Rattei; Fredrik Boulund; Lars Engstrand; Albert Zink; Maria Carmen Collado; Dan R Littman; Daniel Eibach; Danilo Ercolini; Omar Rota-Stabelli; Curtis Huttenhower; Frank Maixner; Nicola Segata

doi:10.1016/j.chom.2019.08.018

The Prevotella copri Complex Comprises Four Distinct Clades Underrepresented in Westernized Populations

Cell Host Microbe. 2019 Nov 13;26(5):666-679.e7. doi: 10.1016/j.chom.2019.08.018. Epub 2019 Oct 10.

Authors

Adrian Tett¹, Kun D Huang², Francesco Asnicar³, Hannah Fehlner-Peach⁴, Edoardo Pasolli³, Nicolai Karcher³, Federica Armanini³, Paolo Manghi³, Kevin Bonham⁵, Moreno Zolfo³, Francesca De Filippis⁶, Cara Magnabosco⁷, Richard Bonneau⁸, John Lusingu⁹, John Amuasi¹⁰, Karl Reinhard¹¹, Thomas Rattei¹², Fredrik Boulund¹³, Lars Engstrand¹⁴, Albert Zink¹⁴, Maria Carmen Collado¹⁵, Dan R Littman⁴, Daniel Eibach¹⁶, Danilo Ercolini⁶, Omar Rota-Stabelli¹⁷, Curtis Huttenhower¹⁸, Frank Maixner¹⁴, Nicola Segata¹⁹

Affiliations

¹ CIBIO Department, University of Trento, 38123 Trento, Italy. Electronic address: [email protected].
² CIBIO Department, University of Trento, 38123 Trento, Italy; Department of Sustainable Agro-Ecosystems and Bioresources, Fondazione Edmund Mach, 1 38010 S, San Michele all'Adige, Italy.
³ CIBIO Department, University of Trento, 38123 Trento, Italy.
⁴ Kimmel Center for Biology and Medicine of the Skirball Institute, New York University School of Medicine, New York, NY 10016, USA.
⁵ The Broad Institute of MIT and Harvard, Cambridge, MA 02115, USA; Department of Agricultural Sciences, University of Naples "Federico II", Portici, Italy.
⁶ Department of Agricultural Sciences, University of Naples "Federico II", Portici, Italy; Task Force on Microbiome Studies, University of Naples "Federico II", Naples, Italy.
⁷ Center for Computational Biology, Flatiron Institute, New York, NY 10010, USA.
⁸ Center for Computational Biology, Flatiron Institute, New York, NY 10010, USA; Departments of Biology and Computer Science, New York University, New York, NY 10003, USA.
⁹ National Institute for Medical Research, Tanga Centre, Tanzania.
¹⁰ Kumasi Centre for Collaborative Research in Tropical Medicine, Kwame Nkrumah University of Science and Technology, Ghana.
¹¹ Hardin Hall, School of Natural Resources, University of Nebraska, Lincoln, NE 68583-0987, USA.
¹² CUBE - Division of Computational Systems Biology, Department of Microbiology and Ecosystem Science, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.
¹³ Centre for Translational Microbiome Research, Department of Microbiology Tumor and Cell Biology, Karolinska Institutet, 171 65 Solna, Stockholm, Sweden.
¹⁴ Institute for Mummy Studies, EURAC Research, Viale Druso 1, 39100 Bolzano, Italy.
¹⁵ Institute of Agrochemistry and Food Technology, National Research Council (IATA-CSIC), 46980 Paterna, Valencia, Spain.
¹⁶ Department of Infectious Disease Epidemiology, Bernhard Nocht Institute for Tropical Medicine, 20359 Hamburg, Germany; German Center for Infection Research, Hamburg-Borstel-Lübeck-Riems, 20359 Hamburg, Germany.
¹⁷ Department of Sustainable Agro-Ecosystems and Bioresources, Fondazione Edmund Mach, 1 38010 S, San Michele all'Adige, Italy.
¹⁸ The Broad Institute of MIT and Harvard, Cambridge, MA 02115, USA; Biostatistics Department, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA.
¹⁹ CIBIO Department, University of Trento, 38123 Trento, Italy. Electronic address: [email protected].

Abstract

Prevotella copri is a common human gut microbe that has been both positively and negatively associated with host health. In a cross-continent meta-analysis exploiting >6,500 metagenomes, we obtained >1,000 genomes and explored the genetic and population structure of P. copri. P. copri encompasses four distinct clades (>10% inter-clade genetic divergence) that we propose constitute the P. copri complex, and all clades were confirmed by isolate sequencing. These clades are nearly ubiquitous and co-present in non-Westernized populations. Genomic analysis showed substantial functional diversity in the complex with notable differences in carbohydrate metabolism, suggesting that multi-generational dietary modifications may be driving reduced prevalence in Westernized populations. Analysis of ancient metagenomes highlighted patterns of P. copri presence consistent with modern non-Westernized populations and a clade delineation time pre-dating human migratory waves out of Africa. These findings reveal that P. copri exhibits a high diversity that is underrepresented in Western-lifestyle populations.

Keywords: Iceman; Prevotella copri; Westernization; ancient DNA; bacterial pangenome; bacterial phylogenetics; comparative microbial genomics; gut microbes; human microbiome; metagenomic assembly; metagenomics.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Diet
Ethiopia
Feces / microbiology
Fossils / microbiology*
Gastrointestinal Microbiome / genetics*
Genetic Variation
Genome, Bacterial / genetics*
Ghana
Humans
Prevotella / classification*
Prevotella / genetics*
Prevotella / isolation & purification
Tanzania

Supplementary concepts

Prevotella copri

Abstract

Publication types

MeSH terms

Supplementary concepts

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