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.

Keywords: Afp; PLTS; PVC; T6SS; bacterial protein translocation; phage tail-like element.

Fig. 1.—

PLTS clusters found in representative genomes of Bacteria and Archaea and the deduced consensus cluster. The conserved genes that are present in all PLTS clusters studied in this report are shown marked in colors, with the exception of PAAR-motif and Mu-gp41-like encoding ORFs that are present only in a number of the examined bacterial genomes. The taxonomic report of the bacterial loci presented in this figure is included in table 1. Gene locus numbers have been included below the first and last ORF of each representative gene cluster.

Fig. 2.—

Phylogenetic relationships of PLTSs in relation with R-type pyocins, P2 and T4 phages, and T6SS. The evolutionary relationships between PLTSs, R-type pyocins, T4 and P2 phages, and T6SS have been constructed using concatenated protein sequences of three common main structural components: gp25, VgrG, and Sheath. The R-type pyocin orthologs are Photorhabdus luminescens: plu3425, plu3427, plu3426, and plu3432; and Pseudomonas entomophila: PSEEN4162, PSEEN4149, PSEEN4163, and PSEEN4155. The T6SS sequences used were Photorhabdus asymbiotica: PAU_00286, PAU_00273, PAU_00288, and PAU_00287; Pectobacterium atrosepticum: ECA3443, ECA3427, ECA3445, and ECA3444; P. asymbiotica: PAU_00286, PAU_00273, PAU_00288, and PAU_00287; and P. entomophila: PSEEN0525, PSEEN0540, PSEEN0523, and PSEEN0523. The corresponding phage protein sequences were retrieved from ViralZone data library (viralzone.expasy.org).

Fig. 3.—

(A) Phylogenetic relationships of the PLTS clusters among prokaryotes based on five concatenated structural gene products. All the PLTS clusters used are listed in table 1. (B) Phylogenetic relationships among the bacteria which carry PLTS, based on 31 concatenated gene products.