A Phage Tail-Derived Element with Wide Distribution among Both Prokaryotic Domains: A Comparative Genomic and Phylogenetic Study

Abstract

Prophage sequences became an integral part of bacterial genomes as a consequence of coevolution, encoding fitness or virulence factors. Such roles have been attributed to phage-derived elements identified in several Gram-negative species: The type VI secretion system (T6SS), the R- and F-type pyocins, and the newly discovered Serratia entomophila antifeeding prophage (Afp), and the Photorhabdus luminescens virulence cassette (PVC). In this study, we provide evidence that remarkably conserved gene clusters, homologous to Afp/PVC, are not restricted to Gram-negative bacteria but are widespread throughout all prokaryotes including the Archaea. Even though they are phylogenetically closer to pyocins, they share key characteristics in common with the T6SS, such as the use of a chaperon-type AAA+ ATPase and the lack of a host cell lysis mechanism. We thus suggest that Afp/PVC-like elements could be classified as phage-like-protein-translocation structures (PLTSs) rather than as pyocins. The reconstruction of phylogeny and the conserved gene content suggest that the diversification of prophage sequences to PLTS occurred in bacteria early in evolution and only once, but PLTS clusters have been horizontally transferred to some of the bacterial lineages and to the Archaea. The adaptation of this element in such a wide host range is suggestive of its versatile use in prokaryotes.

Molecular Analysis of Arthrobacter Myovirus vB_ArtM-ArV1: We Blame It on the Tail

“…Also, HHpred analysis revealed that gp16 of ArV1 may be related to the HCP1 family protein from the type VI secretion system (T6SS) of Acinetobacter baumannii (HHPred probability, 97%; E value, 0.009) and the major tail protein gpV of E. coli phage lambda (HHPred probability, 82%; E value, 12). In type VI secretion systems, HCP1 family proteins are responsible for the formation of the tube (26). Notably, in the case of all three ArV1 gene products discussed above, there was a close match between the position of the protein on the gel and the predicted molecular mass of the protein (Fig.…”

“…According to the literature, all known contractile phage tail-like structures, such as tailed phages, the type VI secretion system (T6SS), R-type pyocins, and phage tail-like protein translocation structures, are multimeric protein complexes that share an architecture and a set of conserved building blocks (26,66,67). All these contractile machineries consist of the main tube, the outer sheath, and the baseplate (26). For many years, bacteriophage T4, the most thoroughly investigated myovirus, served as a model system for all contractile phage tail-like structures.…”

Baseplate assembly of phage Mu: Defining the conserved core components of contractile-tailed phages and related bacterial systems

“…PVCs are a separate class of contractile tail-related apparatuses that have been implicated in killing insect larva and tubeworm morphogenesis (17)(18)(19). We analyzed these because they are more closely related to phage tails than the T6SS, yet display features of a secretion system (3,17). PVC operons were easily identified in bacterial genomes because they encode tail sheath and tube proteins, all six components of the simple contractile baseplate, as well as a distinctive AAA+ ATPase and a unique tail terminator protein (Pfam DUF4255) (3,5,20).…”

“…We analyzed these because they are more closely related to phage tails than the T6SS, yet display features of a secretion system (3,17). PVC operons were easily identified in bacterial genomes because they encode tail sheath and tube proteins, all six components of the simple contractile baseplate, as well as a distinctive AAA+ ATPase and a unique tail terminator protein (Pfam DUF4255) (3,5,20). In analyzing PVC baseplate components using HHpred, we discovered that their BW2 and BW3 proteins could often be strongly linked (probabilities > 90%) to the TssF and TssG protein families (Fig.…”

“…Contractile tails are the most complex type of tail and are associated with phages bearing the largest genomes (1), suggesting that they may be the most powerful phage-genome delivery system. The remarkable capabilities of contractile phage tails are highlighted by the prevalence in bacteria of structures evolved from them, such as the type VI secretion system (T6SS) (2) and Photorhabdus virulence cassettes (PVCs) (3). Thus, characterization of contractile phage tails is vital both to increase our understanding of these complex molecular machines and to provide insight into mechanisms of bacterial pathogenesis.…”