Journal Article

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

VanInsberghe, David, Hussain, Fatima A., Chang, William K., Kelly, Libusha, Yang, Joy, Brown, Julia M., Kauffman, Kathryn M., Sharma, Radhey S., Arevalo, Philip, Cutler, Michael B., Polz, Martin F., Elsherbini, Joseph

2018

Overview

Members of a family of marine dsDNA non-tailed bacterial viruses have short, 10-kb genomes, infect a broader range of hosts than tailed viruses and belong to the double jelly roll capsid lineage of viruses, which are associated with diverse bacterial and archaeal hosts. Microbial predator found in the ocean Double-stranded DNA (dsDNA) viruses comprise both tailed and non-tailed viruses and are thought to be the most abundant viruses on Earth. Tailed viruses of the Caudovirales dominate sequence and culture collections, whereas non-tailed dsDNA viruses often dominate ocean samples but remain largely uncharacterized. Martin Polz and colleagues describe a family of diverse marine non-tailed viruses, called the Autolykiviridae . Through metagenomics and phylogenetic analyses, the team show that Autolykiviridae represent an ancient lineage of double jelly roll capsid viruses. They also show that these viruses are abundant in the ocean, where they prey on marine bacteria and archaea. This finding was facilitated by updated methods for environmental viral discovery, and represents an important step forwards in our understanding of environmental bacteria–virus interactions. The most abundant viruses on Earth are thought to be double-stranded DNA (dsDNA) viruses that infect bacteria 1 . However, tailed bacterial dsDNA viruses ( Caudovirales ), which dominate sequence and culture collections, are not representative of the environmental diversity of viruses 2 , 3 . In fact, non-tailed viruses often dominate ocean samples numerically 4 , 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.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 45 / 45/23 / 45/77 / 631/158/855 / 631/326/432 / 704/158/2446/2447 / Aquatic Organisms - virology / Archaea / Archaea - virology / Bacteria / Bacteria - virology / Bias / Capsid Proteins - metabolism / Culture collections / Deoxyribonucleic acid / DNA / DNA viruses / DNA Viruses - classification / DNA Viruses - genetics / DNA Viruses - isolation & purification / DNA Viruses - pathogenicity / Environment models / Environmental modeling / Gene transfer / Genomes / Health aspects / Host range / Humanities and Social Sciences / letter / Marine bacteria / Marine biology / Metagenomics / Microorganisms / multidisciplinary / Phylogenetics / Phylogeny / Predation / Predators / Proteins / Science / Vibrio / Vibrio - virology / Viral research / Virions / Viruses / Water column / Waterborne diseases