Polyphosphate drives bacterial heterochromatin formation

Beaufay, François; Amemiya, Haley M.; Guan, Jian; Basalla, Joseph; Meinen, Ben A.; Chen, Ziyuan; Mitra, Rishav; Bardwell, James C.A.; Biteen, Julie S.; Vecchiarelli, Anthony G.; Freddolino, Peter L.; Jakob, Ursula

doi:10.1126/sciadv.abk0233

Cited by 44 publications

(45 citation statements)

References 62 publications

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“…On the other hand, the ones that have been known for decades, seem to have an incredibly versatile repertoire of regulatory activities across bacterial species which can expand beyond their interactions with RNA, as shown for Hfq. This pleiotropic regulator has been very recently found to be fundamental for the silencing of prophages and mobile genetic elements by binding to these DNA regions and driving the formation of phase-separated condensates and of heterochromatin-like domains [ 145 ].…”

Section: Discussionmentioning

confidence: 99%

Bacterial RNA chaperones and chaperone-like riboregulators: behind the scenes of RNA-mediated regulation of cellular metabolism

et al. 2022

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In all domains of life, RNA chaperones safeguard and guide the fate of the cellular RNA pool. RNA chaperones comprise structurally diverse proteins that ensure proper folding, stability, and ribonuclease resistance of RNA, and they support regulatory activities mediated by RNA. RNA chaperones constitute a topologically diverse group of proteins that often present an unstructured region and bind RNA with limited nucleotide sequence preferences. In bacteria, three main proteins – Hfq, ProQ, and CsrA – have been shown to regulate numerous complex processes, including bacterial growth, stress response and virulence. Hfq and ProQ have well-studied activities as global chaperones with pleiotropic impact, while CsrA has a chaperone-like role with more defined riboregulatory function. Here, we describe relevant novel insights into their common features, including RNA binding properties, unstructured domains, and interplay with other proteins important to RNA metabolism.

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Section: Discussionmentioning

confidence: 99%

Bacterial RNA chaperones and chaperone-like riboregulators: behind the scenes of RNA-mediated regulation of cellular metabolism

et al. 2022

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“…One class of large subcellular bodies of particular interest in this context are Hfq-based assemblies. Hfq has been suggested to form several types of biomolecular condensates which may have distinct functions in E. coli : two types of RNA-based assemblies, Hfq-foci and H-bodies, both involved in RNA processing during nitrogen starvation, and DNA-based assemblies, specifically the formation of heterochromatin ( 12 , 36 , 37 ). In the context of heterochromatin, Hfq has been shown in vitro to form phase separated assemblies with DNA and polyP ( 12 ).…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, in C. crescentus , it has been shown that disrupting cell cycle progression can in turn alter granule organization ( 6 ). Recently polyP has been suggested to interact with the nucleoid associated protein (NAP) Hfq in Escherichia coli and promote Hfq-mediated transcriptional silencing ( 12 ). Together, these observations indicate that the polyP polymer and polyP granules are structurally and functionally linked to the chromosome in diverse bacterial species.…”

Section: Introductionmentioning

confidence: 99%

The Histone H1-Like Protein AlgP Facilitates Even Spacing of Polyphosphate Granules in Pseudomonas aeruginosa

Chawla

Klupt

Patsalo

et al. 2022

mBio

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“…Inorganic polyphosphate (polyP) is a linear polymer of 3-1000 phosphate units that is produced by organisms of all domains of life [1][2][3]. Bacterial polyP is well known to be important for stress response through diverse mechanisms, including roles in metal chelation [4,5], resistance to oxidants [6], unfolded and damaged protein stabilization [7], and DNA metabolism [8][9][10], and plays a major role in virulence in many pathogens [6,11,12]. Recent work has also begun to decipher the molecular mechanisms by which bacterial polyP directly disrupts phagocytic cell functions important in the host immune response to bacterial infections [13][14][15][16][17].…”

Section: Introductionmentioning

confidence: 99%

The role of nitrogen-responsive regulators in controlling inorganic polyphosphate synthesis in Escherichia coli

et al. 2022

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Inorganic polyphosphate (polyP) is synthesized by bacteria under stressful environmental conditions and acts by a variety of mechanisms to promote cell survival. While the kinase that synthesizes polyP (PPK, encoded by the ppk gene) is well known, ppk transcription is not activated by environmental stress and little is understood about how environmental stress signals lead to polyP accumulation. Previous work has shown that the transcriptional regulators DksA, RpoN (σ54) and RpoE (σ24) positively regulate polyP production, but not ppk transcription, in Escherichia coli . In this work, we examine the role of the alternative sigma factor RpoN and nitrogen starvation stress response pathways in controlling polyP synthesis. We show that the RpoN enhancer binding proteins GlnG and GlrR impact polyP production, and uncover a new role for the nitrogen phosphotransferase regulator PtsN (EIIANtr) as a positive regulator of polyP production, acting upstream of DksA, downstream of RpoN and apparently independently of RpoE. However, neither these regulatory proteins nor common nitrogen metabolites appear to act directly on PPK, and the precise mechanism(s) by which polyP production is modulated after stress remain(s) unclear. Unexpectedly, we also found that the genes that impact polyP production vary depending on the composition of the rich media in which the cells were grown before exposure to polyP-inducing stress. These results constitute progress towards deciphering the regulatory networks driving polyP production under stress, and highlight the remarkable complexity of this regulation and its connections to a broad range of stress-sensing pathways.

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Polyphosphate drives bacterial heterochromatin formation

Abstract: Polyphosphate specifically cooperates with Hfq to silence prophages and mobile genetic elements in the bacterial chromosome.

Cited by 44 publications

References 62 publications

Bacterial RNA chaperones and chaperone-like riboregulators: behind the scenes of RNA-mediated regulation of cellular metabolism

Bacterial RNA chaperones and chaperone-like riboregulators: behind the scenes of RNA-mediated regulation of cellular metabolism

The Histone H1-Like Protein AlgP Facilitates Even Spacing of Polyphosphate Granules in Pseudomonas aeruginosa

The role of nitrogen-responsive regulators in controlling inorganic polyphosphate synthesis in Escherichia coli

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