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Published on: January 26, 2024
Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism
Geeta Ram1, John Chen, Krishan Kumar
1Skirball Institute Program in Molecular Pathogenesis and Department of Microbiology, New York University Medical Center, New York, NY 10016, USA.
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.
Insights
Staphylococcal pathogenicity islands (SaPIs) are mobile genetic elements that spread genes and interfere with helper phage reproduction. They employ diverse strategies, including blocking phage DNA packaging and diverting virion proteins, to ensure their own propagation.
Area of Science:
- Microbiology
- Molecular Biology
- Genetics
Background:
- Staphylococcal pathogenicity islands (SaPIs) are widespread mobile genetic elements in Staphylococcus aureus and other Gram-positive bacteria.
- SaPIs facilitate horizontal gene transfer and act as phage satellites, exploiting temperate helper phages for replication and spread.
Purpose of the Study:
- To investigate the diverse strategies employed by SaPIs to interfere with helper phage reproduction.
- To elucidate the evolutionary mechanisms underlying SaPI persistence and transferability.
Main Methods:
- Analysis of SaPI-encoded proteins and their interactions with phage machinery.
- Characterization of SaPI-mediated interference with phage DNA packaging and virion assembly.
- Comparative genomics to identify conserved and unique interference strategies.
Main Results:
- SaPIs utilize multiple, distinct strategies to inhibit helper phage replication, suggesting convergent evolution.
- One novel strategy involves a SaPI-encoded protein that specifically blocks phage DNA packaging by interfering with the phage terminase small subunit.
- Another strategy involves diverting phage virion proteins for the production of SaPI-specific particles, reducing phage yield.
Conclusions:
- SaPIs have evolved sophisticated mechanisms to interfere with their helper phages, ensuring their own replication and spread.
- These interference strategies, including blocking phage DNA packaging and redirecting virion proteins, are crucial for the evolutionary success of SaPIs.
- Understanding these interactions provides insights into the dynamics of mobile genetic elements and horizontal gene transfer in bacteria.
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