Acetylation of xenogeneic silencer H-NS regulates biofilm development through the nitrogen homeostasis regulator in Shewanella

Abstract Adjusting intracellular metabolic pathways and adopting suitable live state such as biofilms, are crucial for bacteria to survive environmental changes. Although substantial progress has been made in understanding how the histone-like nucleoid-structuring (H-NS) protein modulates the expres...

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Published in:Nucleic acids research 2024-04, Vol.52 (6), p.2886-2903
Main Authors: Liu, Xiaoxiao, Li, Jun, Zhang, Zhixuan, He, Yizhou, Wang, Mingfang, Zhao, Yunhu, Lin, Shituan, Liu, Tianlang, Liao, Yiwen, Zhang, Ni, Yuan, Kaixuan, Ling, Yong, Liu, Ziyao, Chen, Xiaozhong, Chen, Zhe, Chen, Ran, Wang, Xiaoxue, Gu, Bing
Format: Article
Language:English
Subjects:
Acetylation
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biofilms
Glutamine - genetics
Histones - metabolism
Homeostasis
Protein Processing, Post-Translational
Shewanella - genetics
Shewanella - metabolism
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Summary:Abstract Adjusting intracellular metabolic pathways and adopting suitable live state such as biofilms, are crucial for bacteria to survive environmental changes. Although substantial progress has been made in understanding how the histone-like nucleoid-structuring (H-NS) protein modulates the expression of the genes involved in biofilm formation, the precise modification that the H-NS protein undergoes to alter its DNA binding activity is still largely uncharacterized. This study revealed that acetylation of H-NS at Lys19 inhibits biofilm development in Shewanella oneidensis MR-1 by downregulating the expression of glutamine synthetase, a critical enzyme in glutamine synthesis. We further found that nitrogen starvation, a likely condition in biofilm development, induces deacetylation of H-NS and the trimerization of nitrogen assimilation regulator GlnB. The acetylated H-NS strain exhibits significantly lower cellular glutamine concentration, emphasizing the requirement of H-NS deacetylation in Shewanella biofilm development. Moreover, we discovered in vivo that the activation of glutamine biosynthesis pathway and the concurrent suppression of the arginine synthesis pathway during both pellicle and attached biofilms development, further suggesting the importance of fine tune nitrogen assimilation by H-NS acetylation in Shewanella. In summary, posttranslational modification of H-NS endows Shewanella with the ability to respond to environmental needs by adjusting the intracellular metabolism pathways. Graphical Abstract Graphical Abstract
ISSN:0305-1048
1362-4962
DOI:10.1093/nar/gkad1219