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Title: Clades of huge phages from across Earth’s ecosystems

Abstract

Bacteriophages typically have small genomes and depend on their bacterial hosts for replication. Here we sequenced DNA from diverse ecosystems and found hundreds of phage genomes with lengths of more than 200 kilobases (kb), including a genome of 735 kb, which is—to our knowledge—the largest phage genome to be described to date. Thirty-five genomes were manually curated to completion (circular and no gaps). Expanded genetic repertoires include diverse and previously undescribed CRISPR–Cas systems, transfer RNAs (tRNAs), tRNA synthetases, tRNA-modification enzymes, translation-initiation and elongation factors, and ribosomal proteins. The CRISPR–Cas systems of phages 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 phages may repurpose bacterial CRISPR–Cas systems to eliminate competing phages. We phylogenetically define the major clades of huge phages from human and other animal microbiomes, as well as from oceans, lakes, sediments, soils and the built environment. We conclude that the large gene inventories of huge phages reflect a conserved biological strategy, and that the phages are distributed across a broad bacterial host range and across Earth’s ecosystems.

Authors:
 [1];  [1];  [1];  [1];  [2];  [1];  [1];  [1];  [3];  [4];  [1];  [1];  [1];  [1];  [1];  [1];  [5];  [5];  [6];  [3] more »;  [1];  [7];  [1];  [1];  [1];  [1];  [3];  [3];  [3];  [3];  [8];  [1];  [3];  [8];  [9];  [6];  [10];  [11];  [5];  [1];  [12];  [7];  [1];  [13];  [14] « less
+ Show Author Affiliations
  1. Univ. of California, Berkeley, CA (United States). Innovative Genomics Inst.
  2. Technical Univ. of Denmark, Lyngby (Denmark). National Food Inst.
  3. Univ. of California, Berkeley, CA (United States)
  4. Japan Atomic Energy Agency (JAEA), Tokai-mura (Japan). Nuclear Fuel Cycle Engineering Lab.
  5. Stanford Univ., CA (United States). Dept. of Microbiology & Immunology
  6. Colorado State Univ., Fort Collins, CO (United States). Dept. of Soil and Crop Sciences
  7. Univ. of Toronto, ON (Canada). Dept. of Civil and Mineral Engineering
  8. USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
  9. Sun Yat-Sen Univ., Guangzhou (China)
  10. Univ. of Cape Town (South Africa). Centre for Bioprocess Engineering Research
  11. Univ. of Pittsburgh, PA (United States)
  12. Univ. Clermont Auvergne, CNRS, Clermont-Ferrand (France). Lab. Microorganismes: Génome et Environnement
  13. Univ. College London, London (United Kingdom). Inst. of Structural and Molecular Biology
  14. Univ. of California, Berkeley, CA (United States). Innovative Genomics Inst.; Univ. of Melbourne, Melbourne, VIC (Australia)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH); National Science Foundation (NSF); Alfred P. Sloan Foundation; Paul Allen Foundation Frontiers Group; Innovative Genomics Institute; Novo Nordisk Foundation; German Science Foundation; National Research Foundation of South Africa
OSTI Identifier:
1609112
Grant/Contract Number:  
AC02-05CH11231; APSF-2012-10-05; 1349278; GRT00048468; 1342701; CHE-1740549
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 578; Journal Issue: 7795; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Al-Shayeb, Basem, Sachdeva, Rohan, Chen, Lin-Xing, Ward, Fred, Munk, Patrick, Devoto, Audra, Castelle, Cindy J., Olm, Matthew R., Bouma-Gregson, Keith, Amano, Yuki, He, Christine, Méheust, Raphaël, Brooks, Brandon, Thomas, Alex, Lavy, Adi, Matheus-Carnevali, Paula, Sun, Christine, Goltsman, Daniela S. A., Borton, Mikayla A., Sharrar, Allison, Jaffe, Alexander L., Nelson, Tara C., Kantor, Rose, Keren, Ray, Lane, Katherine R., Farag, Ibrahim F., Lei, Shufei, Finstad, Kari, Amundson, Ronald, Anantharaman, Karthik, Zhou, Jinglie, Probst, Alexander J., Power, Mary E., Tringe, Susannah G., Li, Wen-Jun, Wrighton, Kelly, Harrison, Sue, Morowitz, Michael, Relman, David A., Doudna, Jennifer A., Lehours, Anne-Catherine, Warren, Lesley, Cate, Jamie H. D., Santini, Joanne M., and Banfield, Jillian F. Clades of huge phages from across Earth’s ecosystems. United States: N. p., 2020. Web. doi:10.1038/s41586-020-2007-4.
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Al-Shayeb, Basem, Sachdeva, Rohan, Chen, Lin-Xing, Ward, Fred, Munk, Patrick, Devoto, Audra, Castelle, Cindy J., Olm, Matthew R., Bouma-Gregson, Keith, Amano, Yuki, He, Christine, Méheust, Raphaël, Brooks, Brandon, Thomas, Alex, Lavy, Adi, Matheus-Carnevali, Paula, Sun, Christine, Goltsman, Daniela S. A., Borton, Mikayla A., Sharrar, Allison, Jaffe, Alexander L., Nelson, Tara C., Kantor, Rose, Keren, Ray, Lane, Katherine R., Farag, Ibrahim F., Lei, Shufei, Finstad, Kari, Amundson, Ronald, Anantharaman, Karthik, Zhou, Jinglie, Probst, Alexander J., Power, Mary E., Tringe, Susannah G., Li, Wen-Jun, Wrighton, Kelly, Harrison, Sue, Morowitz, Michael, Relman, David A., Doudna, Jennifer A., Lehours, Anne-Catherine, Warren, Lesley, Cate, Jamie H. D., Santini, Joanne M., & Banfield, Jillian F. Clades of huge phages from across Earth’s ecosystems. United States. https://doi.org/10.1038/s41586-020-2007-4
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Al-Shayeb, Basem, Sachdeva, Rohan, Chen, Lin-Xing, Ward, Fred, Munk, Patrick, Devoto, Audra, Castelle, Cindy J., Olm, Matthew R., Bouma-Gregson, Keith, Amano, Yuki, He, Christine, Méheust, Raphaël, Brooks, Brandon, Thomas, Alex, Lavy, Adi, Matheus-Carnevali, Paula, Sun, Christine, Goltsman, Daniela S. A., Borton, Mikayla A., Sharrar, Allison, Jaffe, Alexander L., Nelson, Tara C., Kantor, Rose, Keren, Ray, Lane, Katherine R., Farag, Ibrahim F., Lei, Shufei, Finstad, Kari, Amundson, Ronald, Anantharaman, Karthik, Zhou, Jinglie, Probst, Alexander J., Power, Mary E., Tringe, Susannah G., Li, Wen-Jun, Wrighton, Kelly, Harrison, Sue, Morowitz, Michael, Relman, David A., Doudna, Jennifer A., Lehours, Anne-Catherine, Warren, Lesley, Cate, Jamie H. D., Santini, Joanne M., and Banfield, Jillian F. Wed . "Clades of huge phages from across Earth’s ecosystems". United States. https://doi.org/10.1038/s41586-020-2007-4. https://www.osti.gov/servlets/purl/1609112.
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@article{osti_1609112,
title = {Clades of huge phages from across Earth’s ecosystems},
author = {Al-Shayeb, Basem and Sachdeva, Rohan and Chen, Lin-Xing and Ward, Fred and Munk, Patrick and Devoto, Audra and Castelle, Cindy J. and Olm, Matthew R. and Bouma-Gregson, Keith and Amano, Yuki and He, Christine and Méheust, Raphaël and Brooks, Brandon and Thomas, Alex and Lavy, Adi and Matheus-Carnevali, Paula and Sun, Christine and Goltsman, Daniela S. A. and Borton, Mikayla A. and Sharrar, Allison and Jaffe, Alexander L. and Nelson, Tara C. and Kantor, Rose and Keren, Ray and Lane, Katherine R. and Farag, Ibrahim F. and Lei, Shufei and Finstad, Kari and Amundson, Ronald and Anantharaman, Karthik and Zhou, Jinglie and Probst, Alexander J. and Power, Mary E. and Tringe, Susannah G. and Li, Wen-Jun and Wrighton, Kelly and Harrison, Sue and Morowitz, Michael and Relman, David A. and Doudna, Jennifer A. and Lehours, Anne-Catherine and Warren, Lesley and Cate, Jamie H. D. and Santini, Joanne M. and Banfield, Jillian F.},
abstractNote = {Bacteriophages typically have small genomes and depend on their bacterial hosts for replication. Here we sequenced DNA from diverse ecosystems and found hundreds of phage genomes with lengths of more than 200 kilobases (kb), including a genome of 735 kb, which is—to our knowledge—the largest phage genome to be described to date. Thirty-five genomes were manually curated to completion (circular and no gaps). Expanded genetic repertoires include diverse and previously undescribed CRISPR–Cas systems, transfer RNAs (tRNAs), tRNA synthetases, tRNA-modification enzymes, translation-initiation and elongation factors, and ribosomal proteins. The CRISPR–Cas systems of phages 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 phages may repurpose bacterial CRISPR–Cas systems to eliminate competing phages. We phylogenetically define the major clades of huge phages from human and other animal microbiomes, as well as from oceans, lakes, sediments, soils and the built environment. We conclude that the large gene inventories of huge phages reflect a conserved biological strategy, and that the phages are distributed across a broad bacterial host range and across Earth’s ecosystems.},
doi = {10.1038/s41586-020-2007-4},
journal = {Nature (London)},
number = 7795,
volume = 578,
place = {United States},
year = {Wed Feb 12 00:00:00 EST 2020},
month = {Wed Feb 12 00:00:00 EST 2020}
}
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https://doi.org/10.1038/s41586-020-2007-4
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Figures / Tables:

Fig. 1 Fig. 1: Distribution of the genome sizes and tRNAs of phages. a, Size distribution of circularized bacteriophage genomes from this study, Lak megaphage genomes reported recently for a subset of the same samples and reference sources. Reference genomes were collected from all complete RefSeq r92 dsDNA genomes and non-artefactual assembliesmore » with lengths of more than 200 kb from a previous study. b, Histogram of the genome size distribution of phages with genomes of more than 200 kb from this study, Lak and reference genomes. Box-and-whisker plot of tRNA counts per genome from this study and Lak phages as a function of genome size (Spearman’s ρ = 0.61, P = 4.5 x 10−22, n = 201 individual phage genomes). The middle line for each box marks the median tRNA count for each size bin, the box marks the interquartile range, and the whiskers represent the maximum and minimum.« less
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