Xenogeneic silencing relies on temperature-dependent phosphorylation of the host H-NS protein in Shewanella

Abstract Lateral gene transfer (LGT) plays a key role in shaping the genome evolution and environmental adaptation of bacteria. Xenogeneic silencing is crucial to ensure the safe acquisition of LGT genes into host pre-existing regulatory networks. We previously found that the host nucleoid structuri...

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Bibliographic Details
Published in:Nucleic acids research 2021-04, Vol.49 (6), p.3427-3440
Main Authors: Liu, Xiaoxiao, Lin, Shituan, Liu, Tianlang, Zhou, Yiqing, Wang, Weiquan, Yao, Jianyun, Guo, Yunxue, Tang, Kaihao, Chen, Ran, Benedik, Michael J, Wang, Xiaoxue
Format: Article
Language:English
Subjects:
Bacterial Proteins - chemistry
Bacterial Proteins - metabolism
Cold Shock Proteins and Peptides - genetics
DNA-Binding Proteins - chemistry
DNA-Binding Proteins - metabolism
Gene Silencing
Gene Transfer, Horizontal
Molecular Biology
Phosphoprotein Phosphatases - metabolism
Phosphorylation
Prophages - genetics
Protein Processing, Post-Translational
Protein-Serine-Threonine Kinases - metabolism
Shewanella - genetics
Shewanella - metabolism
Temperature
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Summary:Abstract Lateral gene transfer (LGT) plays a key role in shaping the genome evolution and environmental adaptation of bacteria. Xenogeneic silencing is crucial to ensure the safe acquisition of LGT genes into host pre-existing regulatory networks. We previously found that the host nucleoid structuring protein (H-NS) silences prophage CP4So at warm temperatures yet enables this prophage to excise at cold temperatures in Shewanella oneidensis. However, whether H-NS silences other genes and how bacteria modulate H-NS to regulate the expression of genes have not been fully elucidated. In this study, we discovered that the H-NS silences many LGT genes and the xenogeneic silencing of H-NS relies on a temperature-dependent phosphorylation at warm temperatures in S. oneidensis. Specifically, phosphorylation of H-NS at Ser42 is critical for silencing the cold-inducible genes including the excisionase of CP4So prophage, a cold shock protein, and a stress-related chemosensory system. By contrast, nonphosphorylated H-NS derepresses the promoter activity of these genes/operons to enable their expression at cold temperatures. Taken together, our results reveal that the posttranslational modification of H-NS can function as a regulatory switch to control LGT gene expression in host genomes to enable the host bacterium to react and thrive when environmental temperature changes.
ISSN:0305-1048
1362-4962
DOI:10.1093/nar/gkab137