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

Global phylogeography and ancient evolution of the widespread human gut virus crAssphage
Global phylogeography and ancient evolution of the widespread human gut virus crAssphage
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.
2058-5276
1727-1736
Edwards, R.A.
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Vega, A.A.
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Norman, H.M.
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Ohaeri, M
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Levi, K
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Dinsdale, E A
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Cinek, O
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Aziz, R K
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McNair, K
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Barr, J J
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Bibby, K
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Brouns, Stan JJ
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Cazares, A
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de Jonge, Patrick A
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Desnues, C
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Díaz Munoz, S L
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Fineran, P C
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Kurilshikov, A
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Lavigne, Rob
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Mazankova, K
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McCarthy, D T
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Luzia De Nobrega, Franklin
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Reyes Munoz, A
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Tapia, G
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Trefult, N
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Tyakht, A V
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Vinuesa, P
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Wagemans, J
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Zhernakova, A
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Aarestrup, F M
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Ahmadov, G
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Anton, J
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Cantu, V A
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Cazares, D
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Cho, G S
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Condeff, T
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Cortés, P
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Cranfield, M
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Cuevas, D A
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De la Iglesia, R
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Decewicz, P
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Doane, M P
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Dominy, N J
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Dziewit, L
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Elwasila, B M
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Eren, A M
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Ghedin, E
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Head, S R
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Hill, Colin
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Kelley, S T
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Khan Mirzaei, M
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Kowalewski, M
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Kumaresan, D
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Leigh, S R
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Lipson, D
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Lisitsyna, E S
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Llagostera, M
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Maritz, J M
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Marr, L C
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McCann, A
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Monteiro, S
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Moreira-Grez, S
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Morris, M
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Mugisha, L
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Muniesa, M
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Neve, H
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Nguyen, N P
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Nigro, O D
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Nilsson, A S
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O'Connell, T
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Oliver, A
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Prussin Ii, A J
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Qimron, U
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Quan, Z X
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Rainetova, P
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Ramírez-Rojas, A
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Raya, R
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Reasor, K
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Rice, G A O
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Rossi, A
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Santos, R
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Shimashita, J
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Stachler, E N
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Stene, L C
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Strain, R
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Stumpf, R
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Torres, P J
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Twaddle, A
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Ugochi Ibekwe, M
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Villagra, N
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Wandro, S
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White, B
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Whiteley, A
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Whiteson, K L
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Wijmenga, C
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Zambrano, M M
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Zschach, H
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Dutilh, Bas E.
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et al.
Edwards, R.A.
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Vega, A.A.
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Norman, H.M.
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Ohaeri, M
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Levi, K
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Dinsdale, E A
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Cinek, O
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Aziz, R K
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McNair, K
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Barr, J J
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Bibby, K
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Brouns, Stan JJ
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Cazares, A
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de Jonge, Patrick A
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Desnues, C
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Díaz Munoz, S L
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Fineran, P C
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Kurilshikov, A
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Lavigne, Rob
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Mazankova, K
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McCarthy, D T
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Luzia De Nobrega, Franklin
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Reyes Munoz, A
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Tapia, G
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Trefult, N
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Tyakht, A V
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Vinuesa, P
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Wagemans, J
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Zhernakova, A
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Aarestrup, F M
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Ahmadov, G
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Alassaf, A
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Anton, J
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Asangba, A
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Billings, E K
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Cantu, V A
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Carlton, J M
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Cazares, D
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Cho, G S
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Condeff, T
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Cortés, P
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Cranfield, M
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Cuevas, D A
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De la Iglesia, R
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Decewicz, P
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Doane, M P
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Dominy, N J
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Dziewit, L
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Elwasila, B M
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Eren, A M
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Franz, C
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Fu, J
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Garcia-Aljaro, C
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Ghedin, E
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Gulino, K M
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Haggerty, J M
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Head, S R
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Hendriksen, R S
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Hill, Colin
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Hyoty, H
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Ilina, E N
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Irwin, M T
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Jeffries, T C
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Jofre, J
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Junge, R E
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Kelley, S T
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Khan Mirzaei, M
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Kowalewski, M
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Kumaresan, D
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Leigh, S R
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Lipson, D
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Lisitsyna, E S
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Llagostera, M
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Maritz, J M
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Marr, L C
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McCann, A
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Molshanski-Mor, S
a3cecf0d-ab67-409a-b017-bedeb2f3afaa
Monteiro, S
f00ecd74-d72a-4e2e-b6ea-1c92c0cd446c
Moreira-Grez, S
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Morris, M
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Mugisha, L
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Muniesa, M
1e346928-c330-47ba-a57e-cb6b51bb0876
Neve, H
2ca338f4-4aa8-4458-add9-c53fe6eca84e
Nguyen, N P
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Nigro, O D
dd2026a6-7dce-44bc-8d3f-16570dcdd101
Nilsson, A S
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O'Connell, T
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Odeh, R
b65ca364-b096-46da-995d-61cf47be093a
Oliver, A
02af47d2-19aa-4936-b33e-7684d2c7ec0b
Piuri, M
7826819b-1cb1-44e5-8a4c-9b3d550c82d8
Prussin Ii, A J
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Qimron, U
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Quan, Z X
58b24403-54dd-4f23-85fb-999aef756b8d
Rainetova, P
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Ramírez-Rojas, A
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Raya, R
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Reasor, K
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Rice, G A O
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Rossi, A
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Santos, R
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Shimashita, J
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Stachler, E N
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Stene, L C
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Strain, R
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Stumpf, R
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Torres, P J
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Twaddle, A
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Ugochi Ibekwe, M
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Villagra, N
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Wandro, S
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White, B
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Whiteley, A
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Whiteson, K L
c1ba9c99-0624-48ae-be88-f618f338d6ba
Wijmenga, C
c6e5550a-5d0a-476b-815a-495615e54aca
Zambrano, M M
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Zschach, H
a1d35f75-17e2-4e56-a621-e2f8946d2383
Dutilh, Bas E.
c570f46e-01cb-4c4a-a9bb-3d39b0815106

Edwards, R.A., Vega, A.A. and Norman, H.M. , et al. (2019) Global phylogeography and ancient evolution of the widespread human gut virus crAssphage. Nature Microbiology, 4 (10), 1727-1736. (doi:10.1038/s41564-019-0494-6).

Record type: Article

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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More information

Accepted/In Press date: 22 May 2019
e-pub ahead of print date: 8 July 2019
Published date: October 2019

Identifiers

Local EPrints ID: 443487
URI: http://eprints.soton.ac.uk/id/eprint/443487
DOI: doi:10.1038/s41564-019-0494-6
ISSN: 2058-5276
PURE UUID: 2c4958ef-65ce-4977-ab13-aa896efb14b9
ORCID for Franklin Luzia De Nobrega: ORCID iD orcid.org/0000-0002-8238-1083

Catalogue record

Date deposited: 26 Aug 2020 16:36
Last modified: 17 Mar 2024 04:02

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Contributors

Author: R.A. Edwards
Author: A.A. Vega
Author: H.M. Norman
Author: M Ohaeri
Author: K Levi
Author: E A Dinsdale
Author: O Cinek
Author: R K Aziz
Author: K McNair
Author: J J Barr
Author: K Bibby
Author: Stan JJ Brouns
Author: A Cazares
Author: Patrick A de Jonge
Author: C Desnues
Author: S L Díaz Munoz
Author: P C Fineran
Author: A Kurilshikov
Author: Rob Lavigne
Author: K Mazankova
Author: D T McCarthy
Author: Franklin Luzia De Nobrega ORCID iD
Author: A Reyes Munoz
Author: G Tapia
Author: N Trefult
Author: A V Tyakht
Author: P Vinuesa
Author: J Wagemans
Author: A Zhernakova
Author: F M Aarestrup
Author: G Ahmadov
Author: A Alassaf
Author: J Anton
Author: A Asangba
Author: E K Billings
Author: V A Cantu
Author: J M Carlton
Author: D Cazares
Author: G S Cho
Author: T Condeff
Author: P Cortés
Author: M Cranfield
Author: D A Cuevas
Author: R De la Iglesia
Author: P Decewicz
Author: M P Doane
Author: N J Dominy
Author: L Dziewit
Author: B M Elwasila
Author: A M Eren
Author: C Franz
Author: J Fu
Author: C Garcia-Aljaro
Author: E Ghedin
Author: K M Gulino
Author: J M Haggerty
Author: S R Head
Author: R S Hendriksen
Author: Colin Hill
Author: H Hyoty
Author: E N Ilina
Author: M T Irwin
Author: T C Jeffries
Author: J Jofre
Author: R E Junge
Author: S T Kelley
Author: M Khan Mirzaei
Author: M Kowalewski
Author: D Kumaresan
Author: S R Leigh
Author: D Lipson
Author: E S Lisitsyna
Author: M Llagostera
Author: J M Maritz
Author: L C Marr
Author: A McCann
Author: S Molshanski-Mor
Author: S Monteiro
Author: S Moreira-Grez
Author: M Morris
Author: L Mugisha
Author: M Muniesa
Author: H Neve
Author: N P Nguyen
Author: O D Nigro
Author: A S Nilsson
Author: T O'Connell
Author: R Odeh
Author: A Oliver
Author: M Piuri
Author: A J Prussin Ii
Author: U Qimron
Author: Z X Quan
Author: P Rainetova
Author: A Ramírez-Rojas
Author: R Raya
Author: K Reasor
Author: G A O Rice
Author: A Rossi
Author: R Santos
Author: J Shimashita
Author: E N Stachler
Author: L C Stene
Author: R Strain
Author: R Stumpf
Author: P J Torres
Author: A Twaddle
Author: M Ugochi Ibekwe
Author: N Villagra
Author: S Wandro
Author: B White
Author: A Whiteley
Author: K L Whiteson
Author: C Wijmenga
Author: M M Zambrano
Author: H Zschach
Author: Bas E. Dutilh
Corporate Author: et al.

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