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 Mazankova; David 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

doi:10.1038/s41564-019-0494-6

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

Computational and RNA Biology

49 Citations (Scopus)

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 language	English
Journal	Nature Microbiology
Volume	4
Pages (from-to)	1727-1736
ISSN	2058-5276
DOIs	https://doi.org/10.1038/s41564-019-0494-6
Publication status	Published - 1 Oct 2019

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Edwards, R. A., Vega, A. A., Norman, H. M., Ohaeri, M., Levi, K., Dinsdale, E. A., Cinek, O., Aziz, R. K., McNair, K., Barr, J. J., Bibby, K., Brouns, S. J. J., Cazares, A., de Jonge, P. A., Desnues, C., Díaz Muñoz, S. L., Fineran, P. C., Kurilshikov, A., Lavigne, R., ... Dutilh, B. E. (2019). Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nature Microbiology, 4, 1727-1736. https://doi.org/10.1038/s41564-019-0494-6

Edwards, RA, Vega, AA, Norman, HM, Ohaeri, M, Levi, K, Dinsdale, EA, Cinek, O, Aziz, RK, McNair, K, Barr, JJ, Bibby, K, Brouns, SJJ, Cazares, A, de Jonge, PA, Desnues, C, Díaz Muñoz, SL, Fineran, PC, Kurilshikov, A, Lavigne, R, Mazankova, K, McCarthy, DT, Nobrega, FL, Reyes Muñoz, A, Tapia, G, Trefault, N, Tyakht, AV, Vinuesa, P, Wagemans, J, Zhernakova, A, Aarestrup, FM, Ahmadov, G, Alassaf, A, Anton, J, Asangba, A, Billings, EK, Cantu, VA, Carlton, JM, Cazares, D, Cho, G-S, Condeff, T, Cortés, P, Cranfield, M, Cuevas, DA, De la Iglesia, R, Decewicz, P, Doane, MP, Dominy, NJ, Dziewit, L, Elwasila, BM, Eren, AM, Franz, C, Fu, J, Garcia-Aljaro, C, Ghedin, E, Gulino, KM, Haggerty, JM, Head, SR, Hendriksen, RS, Hill, C, Hyöty, H, Ilina, EN, Irwin, MT, Jeffries, TC, Jofre, J, Junge, RE, Kelley, ST, Khan Mirzaei, M, Kowalewski, M, Kumaresan, D, Leigh, SR, Lipson, D, Lisitsyna, ES, Llagostera, M, Maritz, JM, Marr, LC, McCann, A, Molshanski-Mor, S, Monteiro, S, Moreira-Grez, B, Morris, M, Mugisha, L, Muniesa, M, Neve, H, Nguyen, NP, Nigro, OD, Nilsson, AS, O’Connell, T, Odeh, R, Oliver, A, Piuri, M, Prussin, AJ, Qimron, U, Quan, ZX, Rainetova, P, Ramírez-Rojas, A, Raya, R, Reasor, K, Rice, GAO, Rossi, A, Santos, R, Shimashita, J, Stachler, EN, Stene, LC, Strain, R, Stumpf, R, Torres, PJ, Twaddle, A, Ugochi Ibekwe, MA, Villagra, N, Wandro, S, White, B, Whiteley, A, Whiteson, KL, Wijmenga, C, Zambrano, MM, Zschach, H & Dutilh, BE 2019, 'Global phylogeography and ancient evolution of the widespread human gut virus crAssphage', Nature Microbiology, vol. 4, pp. 1727-1736. https://doi.org/10.1038/s41564-019-0494-6

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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{\textquoteright}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.",

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

year = "2019",

month = oct,

day = "1",

doi = "10.1038/s41564-019-0494-6",

language = "English",

volume = "4",

pages = "1727--1736",

journal = "Nature Microbiology",

issn = "2058-5276",

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TY - JOUR

T1 - Global phylogeography and ancient evolution of the widespread human gut virus crAssphage

AU - Edwards, Robert A.

AU - Vega, Alejandro A.

AU - Norman, Holly M.

AU - Ohaeri, Maria

AU - Levi, Kyle

AU - Dinsdale, Elizabeth A.

AU - Cinek, Ondrej

AU - Aziz, Ramy K.

AU - McNair, Katelyn

AU - Barr, Jeremy J.

AU - Bibby, Kyle

AU - Brouns, Stan J.J.

AU - Cazares, Adrian

AU - de Jonge, Patrick A.

AU - Desnues, Christelle

AU - Díaz Muñoz, Samuel L.

AU - Fineran, Peter C.

AU - Kurilshikov, Alexander

AU - Lavigne, Rob

AU - Mazankova, Karla

AU - McCarthy, David T.

AU - Nobrega, Franklin L.

AU - Reyes Muñoz, Alejandro

AU - Tapia, German

AU - Trefault, Nicole

AU - Tyakht, Alexander V.

AU - Vinuesa, Pablo

AU - Wagemans, Jeroen

AU - Zhernakova, Alexandra

AU - Aarestrup, Frank M.

AU - Ahmadov, Gunduz

AU - Alassaf, Abeer

AU - Anton, Josefa

AU - Asangba, Abigail

AU - Billings, Emma K.

AU - Cantu, Vito Adrian

AU - Carlton, Jane M.

AU - Cazares, Daniel

AU - Cho, Gyu-Sung

AU - Condeff, Tess

AU - Cortés, Pilar

AU - Cranfield, Mike

AU - Cuevas, Daniel A.

AU - De la Iglesia, Rodrigo

AU - Decewicz, Przemyslaw

AU - Doane, Michael P.

AU - Dominy, Nathaniel J.

AU - Dziewit, Lukasz

AU - Elwasila, Bashir Mukhtar

AU - Eren, A. Murat

AU - Franz, Charles

AU - Fu, Jingyuan

AU - Garcia-Aljaro, Cristina

AU - Ghedin, Elodie

AU - Gulino, Kristen M.

AU - Haggerty, John M.

AU - Head, Steven R.

AU - Hendriksen, Rene S.

AU - Hill, Colin

AU - Hyöty, Heikki

AU - Ilina, Elena N.

AU - Irwin, Mitchell T.

AU - Jeffries, Thomas C.

AU - Jofre, Juan

AU - Junge, Randall E.

AU - Kelley, Scott T.

AU - Khan Mirzaei, Mohammadali

AU - Kowalewski, Martin

AU - Kumaresan, Deepak

AU - Leigh, Steven R.

AU - Lipson, David

AU - Lisitsyna, Eugenia S.

AU - Llagostera, Montserrat

AU - Maritz, Julia M.

AU - Marr, Linsey C.

AU - McCann, Angela

AU - Molshanski-Mor, Shahar

AU - Monteiro, Silvia

AU - Moreira-Grez, Benjamin

AU - Morris, Megan

AU - Mugisha, Lawrence

AU - Muniesa, Maite

AU - Neve, Horst

AU - Nguyen, Nam phuong

AU - Nigro, Olivia D.

AU - Nilsson, Anders S.

AU - O’Connell, Taylor

AU - Odeh, Rasha

AU - Oliver, Andrew

AU - Piuri, Mariana

AU - Prussin, Aaron J.

AU - Qimron, Udi

AU - Quan, Zhe Xue

AU - Rainetova, Petra

AU - Ramírez-Rojas, Adán

AU - Raya, Raul

AU - Reasor, Kim

AU - Rice, Gillian A.O.

AU - Rossi, Alessandro

AU - Santos, Ricardo

AU - Shimashita, John

AU - Stachler, Elyse N.

AU - Stene, Lars C.

AU - Strain, Ronan

AU - Stumpf, Rebecca

AU - Torres, Pedro J.

AU - Twaddle, Alan

AU - Ugochi Ibekwe, Mary Ann

AU - Villagra, Nicolás

AU - Wandro, Stephen

AU - White, Bryan

AU - Whiteley, Andy

AU - Whiteson, Katrine L.

AU - Wijmenga, Cisca

AU - Zambrano, Maria M.

AU - Zschach, Henrike

AU - Dutilh, Bas E.

PY - 2019/10/1

Y1 - 2019/10/1

N2 - 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.

AB - 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.

U2 - 10.1038/s41564-019-0494-6

DO - 10.1038/s41564-019-0494-6

M3 - Journal article

C2 - 31285584

AN - SCOPUS:85068899860

SN - 2058-5276

VL - 4

SP - 1727

EP - 1736

JO - Nature Microbiology

JF - Nature Microbiology

ER -

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

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