The evolution of the tape measure protein: units, duplications and losses

Abstract

BackgroundA large family of viruses that infect bacteria, called phages, is characterized by long tails used to inject DNA into their victims' cells. The tape measure protein got its name because the length of the corresponding gene is proportional to the length of the phage's tail: a fact shown by actually copying or splicing out parts of DNA in exemplar species. A natural question is whether there exist units for these tape measures, and if different tape measures have different units and lengths. Such units would allow us to retrace the evolution of tape measure proteins using their duplication/loss history. The vast number of sequenced phages genomes allows us to attack this problem with a comparative genomics approach.ResultsHere we describe a subset of phages whose tape measure proteins contain variable numbers of an 11 amino acids sequence repeat, aligned with sequence similarity, structural properties, and simple arithmetics. This subset provides a unique opportunity for the combinatorial study of phage evolution, without the added uncertainties of multiple alignments, which are trivial in this case, or of protein functions, that are well established. We give a heuristic that reconstructs the duplication history of these sequences, using divergent strains to discriminate between mutations that occurred before and after speciation, or lineage divergence. The heuristic is based on an efficient algorithm that gives an exhaustive enumeration of all possible parsimonious reconstructions of the duplication/speciation history of a single nucleotide. Finally, we present a method that allows, when possible, to discriminate between duplication and loss events.ConclusionsEstablishing the evolutionary history of viruses is difficult, in part due to extensive recombinations and gene transfers, and high mutation rates that often erase detectable similarity between homologous genes. In this paper, we introduce new tools to address this problem.

Functional and structural dissection of the tape measure protein of lactococcal phage TP901-1

“…This is congruent with the work of Katsura and Hendrix who found a similar secondary structure for lambda TMP26. The TMPs of several phages contain (partially) repeated regions with an 11 or 18 aa periodicity and commonly containing aromatic acids at particular positions2728. In the lactococcal phage p2, a 40 amino acid repeat was identified, while the authors suggest that this may be further dissected to an 11 or 11-11-18 residue repeat formation using tryptophan or phenylalanine as a marker, respectively.…”

“…In the lactococcal phage p2, a 40 amino acid repeat was identified, while the authors suggest that this may be further dissected to an 11 or 11-11-18 residue repeat formation using tryptophan or phenylalanine as a marker, respectively. Approximately 5% of phage-encoded TMPs or predicted TMPs examined possessed one or other of these repeat formations27. On this basis, manual alignment of Trp and Phe residues, spaced 11 or 18 amino acids apart, resulted in the identification of 29 proposed aromatic residue-containing repeat sequences (Fig.…”

“…2). The presence of such repeats in TMPs of phages infecting a number of bacterial genera has been defined (approximately 5% of phage proteins assessed)27 and furthermore, the presence of complementary aromatic residues at a similar periodicity in the TMP chaperone of the 936 phage p2 makes it tempting to speculate that these two elements interact via these complementary regions to stabilise the tail assembly process28. However, while these aromatic residues are markers of the proposed repeats, they do not appear to be essential since the replacement of an entire 11 aa repeat with alanine residues bears no impact on the infectivity of the phage (Table 2).…”

Snapshot of haloarchaeal tailed virus genomes

“…TMP are known to evolve by duplications, so the observed repeats could be a trace of this recent evolutionary event in HCTV-1. 66 Tandem repeats seemed to be a non-conserved feature, since even most closely related viruses in our set, HRTV-5 and HRTV-8, showed different patterns of the repeats. In our data set, there was one type of a tandem repeat shared among six viruses.…”

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

“…1, for a myovirus with a medium-sized genome (71 kb), the tail of Arv1 seems to be excessively long (ϳ192 nm) and exhibits a rather unusual mode of sheath contraction. According to the literature, while siphoviruses usually possess longer tails than myoviruses, the length of the tail in both types of phages is determined by the length of the tape measure protein (TMP) (57). While the average lengths of the TMPs of siphophages and myophages are ϳ1,200 and ϳ800 residues, respectively, bacteriophages with larger genomes tend to code for longer TMPs than those with smaller genomes (58).…”