Comparison of the Lysogeny Modules from the TemperateStreptococcus thermophilusBacteriophages TP-J34 and Sfi21: Implications for the Modular Theory of Phage Evolution

Abstract

A 7.6-kb DNA segment covering the putative lysogeny module of the pac-site-containing temperate Streptococcus thermophilus bacteriophage TP-J34 was sequenced. Sequence alignment with the lysogeny module from the cos-site-containing S. thermophilus bacteriophage phiSfi21 revealed areas of high sequence conservation (e.g., over the int gene), interspersed with regions of low or no sequence similarity (e.g., over the cro gene). Four of the six sharp transition zones from high to low sequence conservation were found within open reading frames coding for the CI repressor, the Anti-repressor, the Immunity protein, and a protein of unknown function. The transition points in the cI and ant genes appear to separate gene segments coding for distinct functional domains of these proteins. In addition, these two transition points were located at or near the deletion sites observed in spontaneous phage phiSfi21 deletion mutants, thus suggesting these transition points as recombinational hotspots. Furthermore, the sequence at the transition point in the cI gene resembles the attachment site of the phage, suggesting the involvement of the phage integrase in at least some of the exchange reactions. Contrary to the initial formulation of the modular theory of phage evolution the unit of the evolutionary exchange in streptococcal phages is not a group of functional genes, but can be as small as a single gene. Exchange reactions can also occur within genes, possibly between gene segments encoding distinct protein domains.

Prophage Genomics

“…A lysogenic conversion phenotype was observed for a S. thermophilus strain lysogenic with the prophage TP-J34: it showed distinct growth properties (planktonic versus aggregated growth) when lysogenic or when prophage cured (H. Neve, personal communication). TP-J34 displayed a distinct set of genes between the lysin gene and the attP site (158). A database search revealed that many temperate phages from low-GϩC gram-positive bacteria showed extra genes between the phage lysin and attR (209).…”

Sequence analysis of the lactococcal bacteriophage bIL170: insights into structural proteins and HNH endonucleases in dairy phages The GenBank/EMBL/DDBJ accession numbers for the sequences reported in this paper are bIL170, AF009630; bIL120, AY054975; bIL15, AY054976; bIL191, AY054977; bIL77, AY054978.

“…Since the first proposal of the modular theory of phage evolution in 1980, comparative genomics has highlighted a common scheme of modular genetic organization among various phages infecting Gram-positive or Gram-negative bacteria (Casjens et al, 1992 ;Hendrix et al, 1999) : genes are organized in functional modules (carrying out particular biological functions) that can be exchanged between phages having access to a common gene pool. The modules can be entire sets of genes or single genes, but also gene segments encoding distinct protein domains as already stated for streptococcal phages (Neve et al, 1998). Brussow & Desiere (2001) proposed a lambda supergroup of Siphoviridae, to which the lactococcal phages of the 936 group belong, as well as some other dairy phages occupying the ecological niche of the dairy environment, and for which a relative conservation of gene order was noted, especially in the late cluster.…”

Two Different Panton-Valentine Leukocidin Phage Lineages Predominate in Japan

“…The theory of modular exchange in phages, which is known as the modular theory, has become the basis of a popular hypothesis for phage evolution (26,33). According to this theory, Sa2958 and Sa2mw must share a common ancestor and must have evolved as close relatives, while the module exchange was likely a recent event.…”