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The Prevotella copri complex comprises four distinct clades that are underrepresented in Westernised 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, View ORCID ProfileNicola Segata
doi: https://doi.org/10.1101/600593
Adrian Tett
1CIBIO Department, University of Trento, Italy
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  • For correspondence: adrianjames.tett@unitn.it nicola.segata@unitn.it
Kun D. Huang
1CIBIO Department, University of Trento, Italy
2Department of Sustainable Agro-Ecosystems and Bioresources, Fondazione Edmund Mach, San Michele all’Adige, Italy
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Francesco Asnicar
1CIBIO Department, University of Trento, Italy
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Hannah Fehlner-Peach
3The Kimmel Center for Biology and Medicine of the Skirball Institute, New York University School of Medicine, New York, NY 10016, USA
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Edoardo Pasolli
1CIBIO Department, University of Trento, Italy
4Department of Agricultural Sciences, University of Naples Federico II, Portici, Italy
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Nicolai Karcher
1CIBIO Department, University of Trento, Italy
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Federica Armanini
1CIBIO Department, University of Trento, Italy
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Paolo Manghi
1CIBIO Department, University of Trento, Italy
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Kevin Bonham
5The Broad Institute, Cambridge, USA
6Harvard T.H. Chan School of Public Health, Boston, USA
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Moreno Zolfo
1CIBIO Department, University of Trento, Italy
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Francesca De Filippis
7Department of Agricultural Sciences, University of Naples Federico II, Portici, Italy
8Task Force on Microbiome Studies, University of Naples Federico II, Naples, Italy
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Cara Magnabosco
9Center for Computational Biology, Flatiron Institute, New York, NY 10010, USA
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Richard Bonneau
9Center for Computational Biology, Flatiron Institute, New York, NY 10010, USA
10Departments of Biology and Computer Science, New York University, NY 10003, USA
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John Lusingu
11National Institute for Medical Research, Tanga Centre, Tanzania
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John Amuasi
12Kumasi Centre for Collaborative Research in Tropical Medicine, Kwame Nkrumah University of Science and Technology, Ghana
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Karl Reinhard
13Hardin Hall, School of Natural Resources, University of Nebraska-Lincoln, NE, USA
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Thomas Rattei
14CUBE - Division of Computational Systems Biology, Department of Microbiology and Ecosystem Science, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
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Fredrik Boulund
15Centre for Translational Microbiome Research, Department of Microbiology Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden
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Lars Engstrand
15Centre for Translational Microbiome Research, Department of Microbiology Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden
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Albert Zink
16Institute for Mummy Studies, EURAC Research, Viale Druso 1, 39100 Bolzano, Italy
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Maria Carmen Collado
17Institute of Agrochemistry and Food Technology-National Research Council (IATA-CSIC), 46980, Paterna, Valencia, Spain
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Dan R. Littman
3The Kimmel Center for Biology and Medicine of the Skirball Institute, New York University School of Medicine, New York, NY 10016, USA
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Daniel Eibach
18Department of Infectious Disease Epidemiology, Bernhard Nocht Institute for Tropical Medicine, 20359, Hamburg, Germany
19German Center for Infection Research, Hamburg-Borstel-Lübeck-Riems, 20359, Hamburg, Germany
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Danilo Ercolini
7Department of Agricultural Sciences, University of Naples Federico II, Portici, Italy
8Task Force on Microbiome Studies, University of Naples Federico II, Naples, Italy
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Omar Rota-Stabelli
2Department of Sustainable Agro-Ecosystems and Bioresources, Fondazione Edmund Mach, San Michele all’Adige, Italy
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Curtis Huttenhower
5The Broad Institute, Cambridge, USA
6Harvard T.H. Chan School of Public Health, Boston, USA
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Frank Maixner
16Institute for Mummy Studies, EURAC Research, Viale Druso 1, 39100 Bolzano, Italy
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Nicola Segata
1CIBIO Department, University of Trento, Italy
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  • ORCID record for Nicola Segata
  • For correspondence: adrianjames.tett@unitn.it nicola.segata@unitn.it
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Abstract

Prevotella copri is a common inhabitant of the human gut. Interest in P. copri has gathered pace due to conflicting reports on whether it is beneficial or detrimental to health. In a cross-continent meta-analysis exploiting >6,500 available metagenomes supported by new isolate sequencing and recovery of high-quality genomes from metagenomes, we obtained >1,000 P. copri genomes. This 100-fold increase over existing isolate genomes allowed the genetic and global population structure of P. copri to be explored at an unprecedented depth. We demonstrate P. copri is not a monotypic species, but encompasses four distinct clades (>10% inter-clade vs. <4% intra-clade average single nucleotide variants) for which we propose the name P. copri complex, comprising clades A, B, C and D. We show the complex is near ubiquitous in non-Westernised populations (95.4% versus 29.6% in Westernised populations), where all four clades are typically co-present within an individual (61.6% of the cases), in contrast to Westernised populations (4.6%). Genomic analysis of the complex reveals substantial and complementary functional diversity, including the potential for utilisation of complex carbohydrates, suggestive that multi-generational dietary modifications may be a driver for the reduced P. copri prevalence in Westernised populations. Analysis of ancient stool microbiomes highlights a similar pattern of P. copri presence consistent with modern non-Westernised populations, allowing us to estimate the time of clade delineation to pre-date human migratory waves out of Africa. Our analysis reveals P. copri to be far more diverse than previously appreciated and this diversity appears to be underrepresented in Western-lifestyle populations.

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Posted April 09, 2019.
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The Prevotella copri complex comprises four distinct clades that are underrepresented in Westernised 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
bioRxiv 600593; doi: https://doi.org/10.1101/600593
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The Prevotella copri complex comprises four distinct clades that are underrepresented in Westernised 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
bioRxiv 600593; doi: https://doi.org/10.1101/600593

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