Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism

Abstract

Staphylococcal pathogenicity islands (SaPIs) carry superantigen and resistance genes and are extremely widespread in Staphylococcus aureus and in other Gram-positive bacteria. SaPIs represent a major source of intrageneric horizontal gene transfer and a stealth conduit for intergeneric gene transfer; they are phage satellites that exploit the life cycle of their temperate helper phages with elegant precision to enable their rapid replication and promiscuous spread. SaPIs also interfere with helper phage reproduction, blocking plaque formation, sharply reducing burst size and enhancing the survival of host cells following phage infection. Here, we show that SaPIs use several different strategies for phage interference, presumably the result of convergent evolution. One strategy, not described previously in the bacteriophage microcosm, involves a SaPI-encoded protein that directly and specifically interferes with phage DNA packaging by blocking the phage terminase small subunit. Another strategy involves interference with phage reproduction by diversion of the vast majority of virion proteins to the formation of SaPI-specific small infectious particles. Several SaPIs use both of these strategies, and at least one uses neither but possesses a third. Our studies illuminate a key feature of the evolutionary strategy of these mobile genetic elements, in addition to their carriage of important genes—interference with helper phage reproduction, which could ensure their transferability and long-term persistence.

Bacteriophage-mediated spread of bacterial virulence genes

“…Although in the cos phages (a) the TerL produces a second specific cut in the same cos site, generating unit-length encapsidated molecules, in the pac phages (b) the TerL generates a second cut in a sequence-independent manner only when the propcapsid reaches its capacity. generalized transduction is extremely rare, some mobile genetic elements [30][31][32] have made use of the impressive capabilities of phage particles to transfer DNA both intragenerically and inter-generically [33,34] and have developed elegant strategies to hijack the phage machinery to use for their own benefit [35 ]. The best-characterised elements are the S. aureus pathogenicity islands (SaPIs), which are mobile genetic elements that carry and disseminate superantigen genes, such as toxic shock toxin and enterotoxin B. SaPIs are the prototypical members of the 174 Host-microbe interactions: bacteria …”

Precisely modulated pathogenicity island interference with late phage gene transcription

“…In studies of SaPI interference with helper phage 80 (of the international typing set, a member of the famous 80/81 pair) (8), which is related to but is distinctly different from the more extensively studied 80α, we observed that SaPI2, the major cause of menstrual toxic shock, inhibits phage 80 reproduction more stringently than do other SaPIs, and preliminary results suggested that SaPI2 uses a third interference mechanism (7). In this report we characterize this third interference mechanism used by SaPI2 against phage 80 and other related phages but not against phage 80α.…”

“…The SaPI life cycle is initiated only when the life cycle of a helper phage is in progress; SaPI particle production, however, is not quite able to keep up with helper phage maturation rate, and, perhaps to gain an advantage, SaPIs interfere with the reproduction of their helper phages (7). Thus far, two distinctly different SaPI-coded interference mechanisms have been identified, namely the capsid morphogenesis genes cpmA and B, which cause the formation of small capsids commensurate with the SaPI genome, and the phage packaging inhibition gene ppi, which blocks phage terminase small subunit (TerS P ), favoring the packaging of SaPI DNA.…”

Staphylococcal pathogenicity island DNA packaging system involving cos -site packaging and phage-encoded HNH endonucleases

“…Previously characterized SaPIs and their helper phages use the pac mechanism for DNA encapsidation and encode small terminase subunit (TerS) homologs which complex with the phage-coded large terminase subunit and thus determine SaPI packaging specificity. This process is aided by a SaPI-coded protein, Ppi, which complexes with the phage TerS, blocking its function (1). Many of the SaPIs also encode a capsid morphogenesis module consisting of two proteins, CpmA and -B, which cause the formation of small procapsids that match the smaller size of the SaPI genome (2).…”