Polyamines and linear DNA mediate bacterial threat assessment of bacteriophage infection

Author:

de Mattos Camilla D.1,Faith Dominick R.1,Nemudryi Artem A.2ORCID,Schmidt Amelia K.1,Bublitz DeAnna C.1ORCID,Hammond Lauren3,Kinnersley Margie A.1,Schwartzkopf Caleb M.1,Robinson Autumn J.1ORCID,Joyce Alex1,Michaels Lia A.1,Brzozowski Robert S.1,Coluccio Alison1,Xing Denghui David1ORCID,Uchiyama Jumpei4ORCID,Jennings Laura K.1ORCID,Eswara Prahathees3ORCID,Wiedenheft Blake2ORCID,Secor Patrick R.1ORCID

Affiliation:

1. Division of Biological Sciences, University of Montana, Missoula, MT 59812

2. Department of Microbiology and Cell Biology, Montana State University, Bozeman, MT 59717

3. Department of Cell Biology, Microbiology and Molecular Biology, University of South Florida, Tampa, FL 33620

4. Department of Bacteriology, Graduate School of Medicine Dentistry and Pharmaceutical Sciences, Okayama University, Okayama 700-8558, Japan

Abstract

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.

Funder

HHS | NIH | National Institute of Allergy and Infectious Diseases

HHS | NIH | National Institute of General Medical Sciences

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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