Global phylogeography and ancient evolution of the widespread human gut virus crAssphage

Robert A. Edwards*, Alejandro A. Vega, Holly M. Norman, Maria Ohaeri, Kyle Levi, Elizabeth A. Dinsdale, Ondrej Cinek, Ramy K. Aziz, Katelyn McNair, Jeremy J. Barr, Kyle Bibby, Stan J.J. Brouns, Adrian Cazares, Patrick A. de Jonge, Christelle Desnues, Samuel L. Díaz Muñoz, Peter C. Fineran, Alexander Kurilshikov, Rob Lavigne, Karla MazankovaDavid T. McCarthy, Franklin L. Nobrega, Alejandro Reyes Muñoz, German Tapia, Nicole Trefault, Alexander V. Tyakht, Pablo Vinuesa, Jeroen Wagemans, Alexandra Zhernakova, Frank M. Aarestrup, Gunduz Ahmadov, Abeer Alassaf, Josefa Anton, Abigail Asangba, Emma K. Billings, Vito Adrian Cantu, Jane M. Carlton, Daniel Cazares, Gyu Sung Cho, Tess Condeff, Pilar Cortés, Mike Cranfield, Daniel A. Cuevas, Rodrigo De la Iglesia, Przemyslaw Decewicz, Michael P. Doane, Nathaniel J. Dominy, Lukasz Dziewit, Bashir Mukhtar Elwasila, A. Murat Eren, Charles Franz, Jingyuan Fu, Cristina Garcia-Aljaro, Elodie Ghedin, Kristen M. Gulino, John M. Haggerty, Steven R. Head, Rene S. Hendriksen, Colin Hill, Heikki Hyöty, Elena N. Ilina, Mitchell T. Irwin, Thomas C. Jeffries, Juan Jofre, Randall E. Junge, Scott T. Kelley, Mohammadali Khan Mirzaei, Martin Kowalewski, Deepak Kumaresan, Steven R. Leigh, David Lipson, Eugenia S. Lisitsyna, Montserrat Llagostera, Julia M. Maritz, Linsey C. Marr, Angela McCann, Shahar Molshanski-Mor, Silvia Monteiro, Benjamin Moreira-Grez, Megan Morris, Lawrence Mugisha, Maite Muniesa, Horst Neve, Nam phuong Nguyen, Olivia D. Nigro, Anders S. Nilsson, Taylor O’Connell, Rasha Odeh, Andrew Oliver, Mariana Piuri, Aaron J. Prussin, Udi Qimron, Zhe Xue Quan, Petra Rainetova, Adán Ramírez-Rojas, Raul Raya, Kim Reasor, Gillian A.O. Rice, Alessandro Rossi, Ricardo Santos, John Shimashita, Elyse N. Stachler, Lars C. Stene, Ronan Strain, Rebecca Stumpf, Pedro J. Torres, Alan Twaddle, Mary Ann Ugochi Ibekwe, Nicolás Villagra, Stephen Wandro, Bryan White, Andy Whiteley, Katrine L. Whiteson, Cisca Wijmenga, Maria M. Zambrano, Henrike Zschach, Bas E. Dutilh

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

161 Scopus citations

Abstract

Microbiomes are vast communities of microorganisms and viruses that populate all natural ecosystems. Viruses have been considered to be the most variable component of microbiomes, as supported by virome surveys and examples of high genomic mosaicism. However, recent evidence suggests that the human gut virome is remarkably stable compared with that of other environments. Here, we investigate the origin, evolution and epidemiology of crAssphage, a widespread human gut virus. Through a global collaboration, we obtained DNA sequences of crAssphage from more than one-third of the world’s countries and showed that the phylogeography of crAssphage is locally clustered within countries, cities and individuals. We also found fully colinear crAssphage-like genomes in both Old-World and New-World primates, suggesting that the association of crAssphage with primates may be millions of years old. Finally, by exploiting a large cohort of more than 1,000 individuals, we tested whether crAssphage is associated with bacterial taxonomic groups of the gut microbiome, diverse human health parameters and a wide range of dietary factors. We identified strong correlations with different clades of bacteria that are related to Bacteroidetes and weak associations with several diet categories, but no significant association with health or disease. We conclude that crAssphage is a benign cosmopolitan virus that may have coevolved with the human lineage and is an integral part of the normal human gut virome.

Original languageEnglish
Pages (from-to)1727-1736
Number of pages10
JournalNature Microbiology
Volume4
Issue number10
DOIs
StatePublished - 1 Oct 2019

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