Molecular Piracy: Redirection of Bacteriophage Capsid Assembly by Mobile Genetic Elements

Abstract

Horizontal transfer of mobile genetic elements (MGEs) is a key aspect of the evolution of bacterial pathogens. Transduction by bacteriophages is especially important in this process. Bacteriophages—which assemble a machinery for efficient encapsidation and transfer of genetic material—often transfer MGEs and other chromosomal DNA in a more-or-less nonspecific low-frequency process known as generalized transduction. However, some MGEs have evolved highly specific mechanisms to take advantage of bacteriophages for their own propagation and high-frequency transfer while strongly interfering with phage production—“molecular piracy”. These mechanisms include the ability to sense the presence of a phage entering lytic growth, specific recognition and packaging of MGE genomes into phage capsids, and the redirection of the phage assembly pathway to form capsids with a size more appropriate for the size of the MGE. This review focuses on the process of assembly redirection, which has evolved convergently in many different MGEs from across the bacterial universe. The diverse mechanisms that exist suggest that size redirection is an evolutionarily advantageous strategy for many MGEs.

Assembly-free single-molecule sequencing recovers complete virus genomes from natural microbial communities

“…This mobile element presumably co-opts Pelagibacter phage packaging machinery intracellularly and is consistent with recent reports that pelagiphages in the family Podoviridae integrate into Pelagibacter host genomes (Zhao et al 2019). Although these mobile phage parasites were originally discovered in cultures of Gram-positive bacteria (Ruzin et al 2001;Chen and Novick 2009;Novick et al 2010), more recent studies indicate that PICIs may be much more widespread (Martinez-Rubio et al 2017;Fillol-Salom et al 2018;Dokland 2019). To the best of our knowledge, the results reported here are among the first to show that PICIlike genome concatemers are likely packaged in "wild" phage particles, with concatemer repeat sizes reflecting the genome size of phages they parasitize.…”

The genetic and ecological landscape of plasmids in the human gut

“…Alternatively, these contigs may represent mobile genetic elements with lifestyles that blur the distinctions between categories of horizontally transferred elements. Serendipitous discoveries have given us examples of phages carrying plasmid segregation proteins (Oliva et al 2012) , plasmids encoding capsids ("Characterization of Streptomyces Plasmid-Phage pFP4 and Its Evolutionary Implications" 2012) , and phagemids, which can integrate into the genome like phages or replicate in the cytoplasm like a plasmid (Dokland 2019) . A targeted effort to understand the spectrum of plasmids to phages may reveal many undiscovered mobile genetic elements that do not fall into defined categories.…”

Structure of the Capsid Size-Determining Scaffold of “Satellite” Bacteriophage P4

“…P4 is not considered directly related to the Caudovirales, but appears to be an independent MGE that has acquired some phage-like functions horizontally, allowing it to take advantage of a phage for its dissemination [15,16]. The Sid scaffolding protein has no known analog in phages.…”

“…"Satellite" phage P4 is not a true phage, but rather a "pirate" mobile genetic element (MGE) [15,16]-an integrative plasmid that has acquired the ability to utilize a "helper" phage, such as P2, for its own propagation [17]. When P2 infects a cell harboring a P4 element, trans-activation of P4 by the P2 transcriptional activator Ogr leads to P4 excision (if integrated), replication, and expression of genes involved in trans-regulation of P2, including δ, psu and sid [17].…”