Letter

A major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria

  • Nature volume 554, pages 118122 (01 February 2018)
  • doi:10.1038/nature25474
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Abstract

The most abundant viruses on Earth are thought to be double-stranded DNA (dsDNA) viruses that infect bacteria1. However, tailed bacterial dsDNA viruses (Caudovirales), which dominate sequence and culture collections, are not representative of the environmental diversity of viruses2,3. In fact, non-tailed viruses often dominate ocean samples numerically4, raising the fundamental question of the nature of these viruses. Here we characterize a group of marine dsDNA non-tailed viruses with short 10-kb genomes isolated during a study that quantified the diversity of viruses infecting Vibrionaceae bacteria. These viruses, which we propose to name the Autolykiviridae, represent a novel family within the ancient lineage of double jelly roll (DJR) capsid viruses. Ecologically, members of the Autolykiviridae have a broad host range, killing on average 34 hosts in four Vibrio species, in contrast to tailed viruses which kill on average only two hosts in one species. Biochemical and physical characterization of autolykiviruses reveals multiple virion features that cause systematic loss of DJR viruses in sequencing and culture-based studies, and we describe simple procedural adjustments to recover them. We identify DJR viruses in the genomes of diverse major bacterial and archaeal phyla, and in marine water column and sediment metagenomes, and find that their diversity greatly exceeds the diversity that is currently captured by the three recognized families of such viruses. Overall, these data suggest that viruses of the non-tailed dsDNA DJR lineage are important but often overlooked predators of bacteria and archaea that impose fundamentally different predation and gene transfer regimes on microbial systems than on tailed viruses, which form the basis of all environmental models of bacteria–virus interactions.

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Acknowledgements

We thank J. King, P. Weigele, J. Daily and J. Chodera for comments and suggestions; T. Soni and members of the Polz laboratory for assistance with sampling; S. Labrie for guidance in viral genome extractions and sequencing library preparation, and C. Haase-Pettingell for assistance with density gradients; N. Watson for electron microscopy; and R. Ratzlaff for discussions and the suggestion of electron microscopy of virus plaques in agar overlay. This work was supported by grants from the National Science Foundation OCE 1435993 to M.F.P. and L.K., the NSF GRFP to F.A.H. and the WHOI Ocean Ventures Fund to K.M.K.

Author information

Author notes

    • Julia M. Brown
    •  & Radhey S. Sharma

    Present addresses: Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine 04544, USA (J.M.B.); Department of Environmental Studies, Bioresources & Environmental Biotechnology Laboratory, University of Delhi, Delhi 110007, India (R.S.S.).

Affiliations

  1. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA

    • Kathryn M. Kauffman
    • , Fatima A. Hussain
    • , Joy Yang
    • , Philip Arevalo
    • , David VanInsberghe
    • , Joseph Elsherbini
    • , Radhey S. Sharma
    • , Michael B. Cutler
    •  & Martin F. Polz
  2. Department of Systems and Computational Biology, Albert Einstein College of Medicine, Bronx, New York 10461, USA

    • Julia M. Brown
    • , William K. Chang
    •  & Libusha Kelly

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Contributions

K.M.K., F.A.H., L.K. and M.F.P. designed the study and planned experiments and analyses. K.M.K., L.K. and M.F.P. wrote the paper with contributions from all authors. K.M.K. conducted field sampling, isolations and experimental characterizations of lytic viruses. J.Y. conducted the statistical analyses of the viral decay experiment and wrote the scripts to visualize the infection matrix as a phylogeny-anchored network, which was based on the host ribosomal protein tree generated by P.A. W.K.C. and L.K. performed the quantification of significance of host sharing. F.A.H. performed isolation and characterization of active Vibrio DJR prophages. Bacterial genome sequencing libraries were prepared by M.B.C., assembled by P.A., and curated and annotated by P.A. and J.E. The viral genome sequencing libraries were prepared by K.M.K. and R.S.S., assembled by J.M.B. and K.M.K., and annotated and curated by J.M.B., K.M.K., J.E., W.K.C. and L.K. The viral metagenome sequencing libraries were prepared by K.M.K., and assembled and curated by P.A. and L.K. The bioinformatic analyses of microbial genomes and metagenomes for DJR capsid elements were performed by L.K. and K.M.K., and the visualization of the DJR network was performed by D.V. M.B.C. provided field and laboratory technical support throughout. Although specific contributions are highlighted for each author, all authors contributed in additional ways through contributions to figures, analyses, discussion of results and comments on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Libusha Kelly or Martin F. Polz.

Reviewer Information Nature thanks J. Fuhrman, E. V. Koonin and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Figure 1, a comparison of tailed virus and autolykivirus genome recovery with and without protease treatment. The uncropped source gel for Fig. 3c.

  2. 2.

    Life Sciences Reporting Summary

Excel files

  1. 1.

    Supplementary Data 1

    This file contains accession numbers, taxonomy, and annotation of DJR capsid proteins included in the trees and network.

  2. 2.

    Supplementary Data 2

    This file contains accession numbers, taxonomy, and annotation of DJR capsid proteins included in the trees and network.

  3. 3.

    Supplementary Data 3

    This file contains GenBank accession numbers for newly obtained sequences and previously published genomes included in Fig. 2 and Extended Data Fig. 6.

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