Megaphages infect Prevotella and variants are widespread in gut microbiomes

Audra E. Devoto, Joanne M. Santini, Matthew R. Olm, Karthik Anantharaman, Patrick Munk, Jenny Tung, Elizabeth A. Archie, Peter J. Turnbaugh, Kimberley D. Seed, Ran Blekhman, Frank Møller Aarestrup, Brian C. Thomas, Jillian F. Banfield*

*Corresponding author for this work

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Abstract

Bacteriophages (phages) dramatically shape microbial community composition, redistribute nutrients via host lysis and drive evolution through horizontal gene transfer. Despite their importance, much remains to be learned about phages in the human microbiome. We investigated the gut microbiomes of humans from Bangladesh and Tanzania, two African baboon social groups and Danish pigs; many of these microbiomes contain phages belonging to a clade with genomes >540 kilobases in length, the largest yet reported in the human microbiome and close to the maximum size ever reported for phages. We refer to these as Lak phages. CRISPR spacer targeting indicates that Lak phages infect bacteria of the genus Prevotella. We manually curated to completion 15 distinct Lak phage genomes recovered from metagenomes. The genomes display several interesting features, including use of an alternative genetic code, large intergenic regions that are highly expressed and up to 35 putative transfer RNAs, some of which contain enigmatic introns. Different individuals have distinct phage genotypes, and shifts in variant frequencies over consecutive sampling days reflect changes in the relative abundance of phage subpopulations. Recent homologous recombination has resulted in extensive genome admixture of nine baboon Lak phage populations. We infer that Lak phages are widespread in gut communities that contain the Prevotella species, and conclude that megaphages, with fascinating and underexplored biology, may be common but largely overlooked components of human and animal gut microbiomes.

Original languageEnglish
JournalNature Microbiology
Volume4
Pages (from-to)693-700
ISSN2058-5276
DOIs
Publication statusPublished - 2019

Cite this

Devoto, A. E., Santini, J. M., Olm, M. R., Anantharaman, K., Munk, P., Tung, J., ... Banfield, J. F. (2019). Megaphages infect Prevotella and variants are widespread in gut microbiomes. Nature Microbiology, 4, 693-700. https://doi.org/10.1038/s41564-018-0338-9
Devoto, Audra E. ; Santini, Joanne M. ; Olm, Matthew R. ; Anantharaman, Karthik ; Munk, Patrick ; Tung, Jenny ; Archie, Elizabeth A. ; Turnbaugh, Peter J. ; Seed, Kimberley D. ; Blekhman, Ran ; Møller Aarestrup, Frank ; Thomas, Brian C. ; Banfield, Jillian F. / Megaphages infect Prevotella and variants are widespread in gut microbiomes. In: Nature Microbiology. 2019 ; Vol. 4. pp. 693-700.
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abstract = "Bacteriophages (phages) dramatically shape microbial community composition, redistribute nutrients via host lysis and drive evolution through horizontal gene transfer. Despite their importance, much remains to be learned about phages in the human microbiome. We investigated the gut microbiomes of humans from Bangladesh and Tanzania, two African baboon social groups and Danish pigs; many of these microbiomes contain phages belonging to a clade with genomes >540 kilobases in length, the largest yet reported in the human microbiome and close to the maximum size ever reported for phages. We refer to these as Lak phages. CRISPR spacer targeting indicates that Lak phages infect bacteria of the genus Prevotella. We manually curated to completion 15 distinct Lak phage genomes recovered from metagenomes. The genomes display several interesting features, including use of an alternative genetic code, large intergenic regions that are highly expressed and up to 35 putative transfer RNAs, some of which contain enigmatic introns. Different individuals have distinct phage genotypes, and shifts in variant frequencies over consecutive sampling days reflect changes in the relative abundance of phage subpopulations. Recent homologous recombination has resulted in extensive genome admixture of nine baboon Lak phage populations. We infer that Lak phages are widespread in gut communities that contain the Prevotella species, and conclude that megaphages, with fascinating and underexplored biology, may be common but largely overlooked components of human and animal gut microbiomes.",
author = "Devoto, {Audra E.} and Santini, {Joanne M.} and Olm, {Matthew R.} and Karthik Anantharaman and Patrick Munk and Jenny Tung and Archie, {Elizabeth A.} and Turnbaugh, {Peter J.} and Seed, {Kimberley D.} and Ran Blekhman and {M{\o}ller Aarestrup}, Frank and Thomas, {Brian C.} and Banfield, {Jillian F.}",
year = "2019",
doi = "10.1038/s41564-018-0338-9",
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Devoto, AE, Santini, JM, Olm, MR, Anantharaman, K, Munk, P, Tung, J, Archie, EA, Turnbaugh, PJ, Seed, KD, Blekhman, R, Møller Aarestrup, F, Thomas, BC & Banfield, JF 2019, 'Megaphages infect Prevotella and variants are widespread in gut microbiomes', Nature Microbiology, vol. 4, pp. 693-700. https://doi.org/10.1038/s41564-018-0338-9

Megaphages infect Prevotella and variants are widespread in gut microbiomes. / Devoto, Audra E.; Santini, Joanne M.; Olm, Matthew R.; Anantharaman, Karthik; Munk, Patrick; Tung, Jenny; Archie, Elizabeth A.; Turnbaugh, Peter J.; Seed, Kimberley D.; Blekhman, Ran; Møller Aarestrup, Frank ; Thomas, Brian C.; Banfield, Jillian F.

In: Nature Microbiology, Vol. 4, 2019, p. 693-700.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Megaphages infect Prevotella and variants are widespread in gut microbiomes

AU - Devoto, Audra E.

AU - Santini, Joanne M.

AU - Olm, Matthew R.

AU - Anantharaman, Karthik

AU - Munk, Patrick

AU - Tung, Jenny

AU - Archie, Elizabeth A.

AU - Turnbaugh, Peter J.

AU - Seed, Kimberley D.

AU - Blekhman, Ran

AU - Møller Aarestrup, Frank

AU - Thomas, Brian C.

AU - Banfield, Jillian F.

PY - 2019

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N2 - Bacteriophages (phages) dramatically shape microbial community composition, redistribute nutrients via host lysis and drive evolution through horizontal gene transfer. Despite their importance, much remains to be learned about phages in the human microbiome. We investigated the gut microbiomes of humans from Bangladesh and Tanzania, two African baboon social groups and Danish pigs; many of these microbiomes contain phages belonging to a clade with genomes >540 kilobases in length, the largest yet reported in the human microbiome and close to the maximum size ever reported for phages. We refer to these as Lak phages. CRISPR spacer targeting indicates that Lak phages infect bacteria of the genus Prevotella. We manually curated to completion 15 distinct Lak phage genomes recovered from metagenomes. The genomes display several interesting features, including use of an alternative genetic code, large intergenic regions that are highly expressed and up to 35 putative transfer RNAs, some of which contain enigmatic introns. Different individuals have distinct phage genotypes, and shifts in variant frequencies over consecutive sampling days reflect changes in the relative abundance of phage subpopulations. Recent homologous recombination has resulted in extensive genome admixture of nine baboon Lak phage populations. We infer that Lak phages are widespread in gut communities that contain the Prevotella species, and conclude that megaphages, with fascinating and underexplored biology, may be common but largely overlooked components of human and animal gut microbiomes.

AB - Bacteriophages (phages) dramatically shape microbial community composition, redistribute nutrients via host lysis and drive evolution through horizontal gene transfer. Despite their importance, much remains to be learned about phages in the human microbiome. We investigated the gut microbiomes of humans from Bangladesh and Tanzania, two African baboon social groups and Danish pigs; many of these microbiomes contain phages belonging to a clade with genomes >540 kilobases in length, the largest yet reported in the human microbiome and close to the maximum size ever reported for phages. We refer to these as Lak phages. CRISPR spacer targeting indicates that Lak phages infect bacteria of the genus Prevotella. We manually curated to completion 15 distinct Lak phage genomes recovered from metagenomes. The genomes display several interesting features, including use of an alternative genetic code, large intergenic regions that are highly expressed and up to 35 putative transfer RNAs, some of which contain enigmatic introns. Different individuals have distinct phage genotypes, and shifts in variant frequencies over consecutive sampling days reflect changes in the relative abundance of phage subpopulations. Recent homologous recombination has resulted in extensive genome admixture of nine baboon Lak phage populations. We infer that Lak phages are widespread in gut communities that contain the Prevotella species, and conclude that megaphages, with fascinating and underexplored biology, may be common but largely overlooked components of human and animal gut microbiomes.

U2 - 10.1038/s41564-018-0338-9

DO - 10.1038/s41564-018-0338-9

M3 - Journal article

C2 - 30692672

AN - SCOPUS:85060806368

VL - 4

SP - 693

EP - 700

JO - Nature Microbiology

JF - Nature Microbiology

SN - 2058-5276

ER -