TitleA major lineage of non-tailed dsDNA viruses as unrecognized killers of marine bacteria.
Publication TypeJournal Article
AuthorsKauffman KM, Hussain FA, Yang J, Arevalo P, Brown JM, Chang WK, VanInsberghe D, Elsherbini J, Sharma RS, Cutler MB, Kelly L, Polz MF
Date2018 Feb 01

The most abundant viruses on Earth are thought to be double-stranded DNA (dsDNA) viruses that infect bacteria. However, tailed bacterial dsDNA viruses (Caudovirales), which dominate sequence and culture collections, are not representative of the environmental diversity of viruses. In fact, non-tailed viruses often dominate ocean samples numerically, 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.

Alternate JournalNature
PubMed ID29364876
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    Parsons Laboratory
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    <p><strong>Professor Martin Polz</strong><br>Ralph M. Parsons Laboratory for Environmental Science and Engineering<br>Massachusetts Institute of Technology<br>15 Vassar Street, Bldg 48-417<br>Cambridge, MA 02139</p>
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    Microbial Ecology and Evolution
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    Environmental microbiology is at an important crossroads. Over the last twenty years we have learned that microbes are the most ubiquitous organisms on Earth, yet the dynamics that govern their interactions and evolution remain poorly understood. What is the role of individual populations within the community? What is the range of genomic similarity that defines a population as a functional unit? What mechanisms govern diversification of microbial populations in the environment?

    We address these questions using a combination of quantitative molecular approaches, genomics, physiology, and modeling. Our primary model system is the coastal ocean where we study patterns of diversity among co-occurring bacterioplankton from the level of the entire community to the individual genome. For the latter, we focus on bacteria of the genus Vibrio, which are longstanding models of heterotrophic, marine bacteria and also contain many pathogenic variants (e.g., V. choleraeV. vulnificus). As part of the Woods Hole Center for Oceans and Human Health (COHH), we are also exploring environmental and evolutionary mechanisms that trigger the emergence of pathogenic variants within the vibrios.  We are also part of the Earth Systems Initiative and the Microbial Systems Group at MIT.

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