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

Research output: Contribution to journalArticle

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

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Phylogeography
Viruses
Microbiota
Primates
Bacteroidetes
Mosaicism
Health
Developing Countries
Ecosystem
Epidemiology
Genome
Diet
Bacteria

ASJC Scopus subject areas

  • Microbiology
  • Immunology
  • Applied Microbiology and Biotechnology
  • Genetics
  • Microbiology (medical)
  • Cell Biology

Cite this

Edwards, R. A., Vega, A. A., Norman, H. M., Ohaeri, M., Levi, K., Dinsdale, E. A., ... Dutilh, B. E. (2019). Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nature Microbiology, 4(10), 1727-1736. https://doi.org/10.1038/s41564-019-0494-6

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

In: Nature Microbiology, Vol. 4, No. 10, 01.10.2019, p. 1727-1736.

Research output: Contribution to journalArticle

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, GS, 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, no. 10, pp. 1727-1736. https://doi.org/10.1038/s41564-019-0494-6
Edwards RA, Vega AA, Norman HM, Ohaeri M, Levi K, Dinsdale EA et al. Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nature Microbiology. 2019 Oct 1;4(10):1727-1736. https://doi.org/10.1038/s41564-019-0494-6
Edwards, Robert A. ; Vega, Alejandro A. ; Norman, Holly M. ; Ohaeri, Maria ; Levi, Kyle ; Dinsdale, Elizabeth A. ; Cinek, Ondrej ; Aziz, Ramy K. ; McNair, Katelyn ; Barr, Jeremy J. ; Bibby, Kyle ; Brouns, Stan J.J. ; Cazares, Adrian ; de Jonge, Patrick A. ; Desnues, Christelle ; Díaz Muñoz, Samuel L. ; Fineran, Peter C. ; Kurilshikov, Alexander ; Lavigne, Rob ; Mazankova, Karla ; McCarthy, David T. ; Nobrega, Franklin L. ; Reyes Muñoz, Alejandro ; Tapia, German ; Trefault, Nicole ; Tyakht, Alexander V. ; Vinuesa, Pablo ; Wagemans, Jeroen ; Zhernakova, Alexandra ; Aarestrup, Frank M. ; Ahmadov, Gunduz ; Alassaf, Abeer ; Anton, Josefa ; Asangba, Abigail ; Billings, Emma K. ; Cantu, Vito Adrian ; Carlton, Jane M. ; Cazares, Daniel ; Cho, Gyu Sung ; Condeff, Tess ; Cortés, Pilar ; Cranfield, Mike ; Cuevas, Daniel A. ; De la Iglesia, Rodrigo ; Decewicz, Przemyslaw ; Doane, Michael P. ; Dominy, Nathaniel J. ; Dziewit, Lukasz ; Elwasila, Bashir Mukhtar ; Eren, A. Murat ; Franz, Charles ; Fu, Jingyuan ; Garcia-Aljaro, Cristina ; Ghedin, Elodie ; Gulino, Kristen M. ; Haggerty, John M. ; Head, Steven R. ; Hendriksen, Rene S. ; Hill, Colin ; Hyöty, Heikki ; Ilina, Elena N. ; Irwin, Mitchell T. ; Jeffries, Thomas C. ; Jofre, Juan ; Junge, Randall E. ; Kelley, Scott T. ; Khan Mirzaei, Mohammadali ; Kowalewski, Martin ; Kumaresan, Deepak ; Leigh, Steven R. ; Lipson, David ; Lisitsyna, Eugenia S. ; Llagostera, Montserrat ; Maritz, Julia M. ; Marr, Linsey C. ; McCann, Angela ; Molshanski-Mor, Shahar ; Monteiro, Silvia ; Moreira-Grez, Benjamin ; Morris, Megan ; Mugisha, Lawrence ; Muniesa, Maite ; Neve, Horst ; Nguyen, Nam phuong ; Nigro, Olivia D. ; Nilsson, Anders S. ; O’Connell, Taylor ; Odeh, Rasha ; Oliver, Andrew ; Piuri, Mariana ; Prussin, Aaron J. ; Qimron, Udi ; Quan, Zhe Xue ; Rainetova, Petra ; Ramírez-Rojas, Adán ; Raya, Raul ; Reasor, Kim ; Rice, Gillian A.O. ; Rossi, Alessandro ; Santos, Ricardo ; Shimashita, John ; Stachler, Elyse N. ; Stene, Lars C. ; Strain, Ronan ; Stumpf, Rebecca ; Torres, Pedro J. ; Twaddle, Alan ; Ugochi Ibekwe, Mary Ann ; Villagra, Nicolás ; Wandro, Stephen ; White, Bryan ; Whiteley, Andy ; Whiteson, Katrine L. ; Wijmenga, Cisca ; Zambrano, Maria M. ; Zschach, Henrike ; Dutilh, Bas E. / Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. In: Nature Microbiology. 2019 ; Vol. 4, No. 10. pp. 1727-1736.
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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’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.",
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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.

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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.

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