Polyamines and linear DNA mediate bacterial threat assessment of bacteriophage infection.

Polyamines and linear DNA mediate bacterial threat assessment of bacteriophage infection.
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DOI:
10.1073/pnas.2216430120
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发表时间:
2023-02-28
影响因子:
11.1
通讯作者:
Secor, Patrick R.
Secor, Patrick R.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
de Mattos, Camilla D.;Faith, Dominick R.;Nemudryi, Artem A.;Schmidt, Amelia K.;Bublitz, DeAnna C.;Hammond, Lauren;Kinnersley, Margie A.;Schwartzkopf, Caleb M.;Robinson, Autumn J.;Joyce, Alex;Michaels, Lia A.;Brzozowski, Robert S.;Coluccio, Alison;Xing, Denghui David;Uchiyama, Jumpei;Jennings, Laura K.;Eswara, Prahathees;Wiedenheft, Blake;Secor, Patrick R.

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When cells lyse, danger signals are released into the environment that warn adjacent cells of nearby danger. However, the molecules that serve as bacterial danger signals are poorly defined, and how danger signals affect bacterial responses to threats such as bacteriophage infection are unknown. Here, we demonstrate that polyamines released by lysed bacteria are internalized by adjacent cells. In the absence of bacteriophage infection, intracellular polyamine levels quickly return to baseline. When bacteriophage infect a cell, they inject linear DNA that causes intracellular polyamine levels to remain high, interfering with bacteriophage DNA replication. Our results indicate that polyamines released by lysed cells and linear DNA associated with bacteriophage infection are danger signals that guide bacterial threat assessment of bacteriophage infection. Monitoring the extracellular environment for danger signals is a critical aspect of cellular survival. However, the danger signals released by dying bacteria and the mechanisms bacteria use for threat assessment remain largely unexplored. Here, we show that lysis of Pseudomonas aeruginosa cells releases polyamines that are subsequently taken up by surviving cells via a mechanism that relies on Gac/Rsm signaling. While intracellular polyamines spike in surviving cells, the duration of this spike varies according to the infection status of the cell. In bacteriophage-infected cells, intracellular polyamines are maintained at high levels, which inhibits replication of the bacteriophage genome. Many bacteriophages package linear DNA genomes and linear DNA is sufficient to trigger intracellular polyamine accumulation, suggesting that linear DNA is sensed as a second danger signal. Collectively, these results demonstrate how polyamines released by dying cells together with linear DNA allow P. aeruginosa to make threat assessments of cellular injury.
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