Enteric Chromosomal Islands: DNA Packaging Specificity and Role of λ-like Helper Phage Terminase

Abstract

The phage-inducible chromosomal islands (PICIs) of Gram-negative bacteria are analogous to defective prophages that have lost the ability to propagate without the aid of a helper phage. PICIs have acquired genes that alter the genetic repertoire of the bacterial host, including supplying virulence factors. Recent work by the Penadés laboratory elucidates how a helper phage infection or prophage induction induces the island to excise from the bacterial chromosome, replicate, and become packaged into functional virions. PICIs lack a complete set of morphogenetic genes needed to construct mature virus particles. Rather, PICIs hijack virion assembly functions from an induced prophage acting as a helper phage. The hijacking strategy includes preventing the helper phage from packaging its own DNA while enabling PICI DNA packaging. In the case of recently described Gram-negative PICIs, the PICI changes the specificity of DNA packaging. This is achieved by an island-encoded protein (Rpp) that binds to the phage protein (TerS), which normally selects phage DNA for packaging from a DNA pool that includes the helper phage and host DNAs. The Rpp–TerS interaction prevents phage DNA packaging while sponsoring PICI DNA packaging. Our communication reviews published data about the hijacking mechanism and its implications for phage DNA packaging. We propose that the Rpp–TerS complex binds to a site in the island DNA that is positioned analogous to that of the phage DNA but has a completely different sequence. The critical role of TerS in the Rpp–TerS complex is to escort TerL to the PICI cosN, ensuring appropriate DNA cutting and packaging.

Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements

“…Together with the correspondence of viral genome and VEIME concatemer size ranges ( Fig. 1 B ), these data suggest that capsid remodeling (and concomitant capsid size reduction) is not a common strategy among these marine VEIMEs, as it is in most previously described gram-positive and gram-negative phage satellite systems ( 6 , 10 , 17 , 21 ).…”

Marine viral particles reveal an expansive repertoire of phage-parasitizing mobile elements

“…Together with the correspondence of viral genome and VEIME concatemer size ranges (Fig. 1B), these data suggest that capsid remodeling (and concomitant capsid size reduction) is not as common a strategy in marine VEIMEs, as it is for previously described Gram-positive and Gram-negative phage satellite systems (6, 10, 18, 21).…”

A Perspective on Studies of Phage DNA Packaging Dynamics

“…Packaging of this type occurs in viruses with both double-stranded RNA and double-stranded DNA genomes. An attraction for studying this process is that it is complex enough to be biological (includes energy transduction via ATP cleavage), but simple enough so that one can envisage using current technology to obtain a thorough answer to the question of how it occurs (reviews [ 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 ]). As I discuss below, an additional attraction for me is that I can imagine that, from studies of phage nucleic acid packaging, solutions to key problems of biomedicine will evolve.…”

“…These experiments attracted others into pursuit of the details of DNA packaging. One of the first details learned was that the capsid of the mature phage was physically and chemically different from its procapsid precursor (reviews [ 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 ]).…”

“…However, from studies of phage nucleic acid packaging, we know that all double-stranded DNA and RNA phages have procapsids and mature capsids with a nucleic acid-entry portal [ 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 ], potentially useful as a DDV-gate. This portal is discussed in the articles presented here.…”