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Clades of huge phage from across Earth’s ecosystems

Basem Al-Shayeb, View ORCID ProfileRohan Sachdeva, View ORCID ProfileLin-Xing Chen, Fred Ward, Patrick Munk, Audra Devoto, Cindy J. Castelle, Matthew R. Olm, Keith Bouma-Gregson, Yuki Amano, Christine He, View ORCID ProfileRaphaël Méheust, Brandon Brooks, Alex Thomas, Adi Lavy, Paula Matheus-Carnevali, Christine Sun, Daniela S. A. Goltsman, Mikayla A. Borton, Tara C. Nelson, Rose Kantor, Alexander L. Jaffe, Ray Keren, Ibrahim F. Farag, Shufei Lei, Kari Finstad, Ronald Amundson, Karthik Anantharaman, Jinglie Zhou, Alexander J. Probst, Mary E. Power, Susannah G. Tringe, Wen-Jun Li, Kelly Wrighton, Sue Harrison, Michael Morowitz, David A. Relman, Jennifer A Doudna, Anne-Catherine Lehours, Lesley Warren, Jamie H. D. Cate, Joanne M. Santini, View ORCID ProfileJillian F. Banfield
doi: https://doi.org/10.1101/572362
Basem Al-Shayeb
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Rohan Sachdeva
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Lin-Xing Chen
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Fred Ward
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Patrick Munk
2National Food Institute, Technical University of Denmark, Kongens Lyngby, Denmark
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Audra Devoto
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Cindy J. Castelle
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Matthew R. Olm
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Keith Bouma-Gregson
3Earth and Planetary Science, University of California, Berkeley, CA, USA
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Yuki Amano
4Japan Atomic Energy Agency, Tokai-mura, Japan
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Christine He
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Raphaël Méheust
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Brandon Brooks
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Alex Thomas
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Adi Lavy
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Paula Matheus-Carnevali
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Christine Sun
5Stanford University, California, 94305 USA
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Daniela S. A. Goltsman
5Stanford University, California, 94305 USA
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Mikayla A. Borton
6Colorado State University, Colorado, USA 80521
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Tara C. Nelson
7University of Toronto, Canada
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Rose Kantor
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Alexander L. Jaffe
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Ray Keren
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Ibrahim F. Farag
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Shufei Lei
3Earth and Planetary Science, University of California, Berkeley, CA, USA
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Kari Finstad
8Environmental Science, Policy and Management, University of California, Berkeley, 94720, California, USA
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Ronald Amundson
8Environmental Science, Policy and Management, University of California, Berkeley, 94720, California, USA
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Karthik Anantharaman
3Earth and Planetary Science, University of California, Berkeley, CA, USA
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Jinglie Zhou
9DOE Joint Genome Institute, Walnut Creek, California, USA
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Alexander J. Probst
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Mary E. Power
10Integrative Biology, University of California, Berkeley, 94720, California, USA
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Susannah G. Tringe
9DOE Joint Genome Institute, Walnut Creek, California, USA
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Wen-Jun Li
11Sun Yat-Sen University, Guangzhou 510275, PR China
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Kelly Wrighton
6Colorado State University, Colorado, USA 80521
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Sue Harrison
12Centre for Bioprocess Engineering Research, University of Cape Town, Rondebosch 7701, South Africa
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Michael Morowitz
13University of Pittsburgh School of Medicine, Pittsburgh, PA 15261
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David A. Relman
5Stanford University, California, 94305 USA
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Jennifer A Doudna
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Anne-Catherine Lehours
14Université Clermont Auvergne, CNRS, F-63000, Clermont-Ferrand, France
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Lesley Warren
7University of Toronto, Canada
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Jamie H. D. Cate
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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Joanne M. Santini
15Institute of Structural and Molecular Biology, University College London, WC1E 6BT UK
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Jillian F. Banfield
1Innovative Genomics Institute, University of California, Berkeley, 94720, California, USA
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  • ORCID record for Jillian F. Banfield
  • For correspondence: jbanfield@berkeley.edu
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Abstract

Phage typically have small genomes and depend on their bacterial hosts for replication. DNA sequenced from many diverse ecosystems revealed hundreds of huge phage genomes, between 200 kbp and 716 kbp in length. Thirty-four genomes were manually curated to completion, including the largest phage genomes yet reported. Expanded genetic repertoires include diverse and new CRISPR-Cas systems, tRNAs, tRNA synthetases, tRNA modification enzymes, translation initiation and elongation factors, and ribosomal proteins. Phage CRISPR-Cas systems have the capacity to silence host transcription factors and translational genes, potentially as part of a larger interaction network that intercepts translation to redirect biosynthesis to phage-encoded functions. In addition, some phage may repurpose bacterial CRISPR-Cas systems to eliminate competing phage. We phylogenetically define major clades of huge phage from human and other animal microbiomes, oceans, lakes, sediments, soils and the built environment. We conclude that their large gene inventories reflect a conserved biological strategy, observed over a broad bacterial host range and across Earth’s ecosystems.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted March 11, 2019.
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Clades of huge phage from across Earth’s ecosystems
Basem Al-Shayeb, Rohan Sachdeva, Lin-Xing Chen, Fred Ward, Patrick Munk, Audra Devoto, Cindy J. Castelle, Matthew R. Olm, Keith Bouma-Gregson, Yuki Amano, Christine He, Raphaël Méheust, Brandon Brooks, Alex Thomas, Adi Lavy, Paula Matheus-Carnevali, Christine Sun, Daniela S. A. Goltsman, Mikayla A. Borton, Tara C. Nelson, Rose Kantor, Alexander L. Jaffe, Ray Keren, Ibrahim F. Farag, Shufei Lei, Kari Finstad, Ronald Amundson, Karthik Anantharaman, Jinglie Zhou, Alexander J. Probst, Mary E. Power, Susannah G. Tringe, Wen-Jun Li, Kelly Wrighton, Sue Harrison, Michael Morowitz, David A. Relman, Jennifer A Doudna, Anne-Catherine Lehours, Lesley Warren, Jamie H. D. Cate, Joanne M. Santini, Jillian F. Banfield
bioRxiv 572362; doi: https://doi.org/10.1101/572362
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Clades of huge phage from across Earth’s ecosystems
Basem Al-Shayeb, Rohan Sachdeva, Lin-Xing Chen, Fred Ward, Patrick Munk, Audra Devoto, Cindy J. Castelle, Matthew R. Olm, Keith Bouma-Gregson, Yuki Amano, Christine He, Raphaël Méheust, Brandon Brooks, Alex Thomas, Adi Lavy, Paula Matheus-Carnevali, Christine Sun, Daniela S. A. Goltsman, Mikayla A. Borton, Tara C. Nelson, Rose Kantor, Alexander L. Jaffe, Ray Keren, Ibrahim F. Farag, Shufei Lei, Kari Finstad, Ronald Amundson, Karthik Anantharaman, Jinglie Zhou, Alexander J. Probst, Mary E. Power, Susannah G. Tringe, Wen-Jun Li, Kelly Wrighton, Sue Harrison, Michael Morowitz, David A. Relman, Jennifer A Doudna, Anne-Catherine Lehours, Lesley Warren, Jamie H. D. Cate, Joanne M. Santini, Jillian F. Banfield
bioRxiv 572362; doi: https://doi.org/10.1101/572362

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