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R-DeeP/TripepSVM identifies the RNA-binding OB-fold-like protein PatR as regulator of heterocyst patterning

ABSTRACT: RNA-binding proteins (RBPs) are central components of gene regulatory networks. The differentiation of heterocysts in filamentous cyanobacteria is an example of cell differentiation in prokaryotes. Although multiple non-coding transcripts are involved in this process, no RBPs have been implicated thus far. Here we used quantitative mass spectrometry to analyze the differential fractionation of RNA-protein complexes after RNase treatment in density gradients yielding 333 RNA-associated proteins, while a bioinformatic prediction yielded 311 RBP candidates in Nostoc sp. PCC 7120. We validated in vivo the RNA-binding capacity of 6 RBP candidates. Alr1700 is an RBP with two OB-fold domains that is differentially expressed in heterocysts and interacts with non-coding regulatory RNAs. Deletion of alr1700 led to complete deregulation of the cell differentiation process, a striking increase in the number of heterocyst-like cells, and was ultimately lethal in the absence of combined nitrogen. These observations characterize this RBP as a master regulator of the heterocyst patterning and differentiation process, leading us to rename Alr1700 to PatR.

ORGANISM(S): Nostoc sp. PCC 7120 = FACHB-418

PROVIDER: GSE280056 | GEO | 2024/12/20

REPOSITORIES: GEO

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A new world of RNA-binding proteins in heterocyst-forming cyanobacteria.

Project description:RNA-binding proteins (RBPs) are central components of gene regulatory networks and RNA metabolism. The differentiation of nitrogen-fixing heterocysts in some filamentous cyanobacteria and their cooperation with vegetative cells in the same filament is one of the evolutionarily oldest cases of true multicellularity. Nostoc sp. PCC 7120 (Nostoc) is a model organism for filamentous cyanobacteria that differentiate heterocysts. Although hundreds of noncoding transcripts may be involved in this process, the RBPs that could cooperate with them are poorly characterized. We have used R-DeeP/GradR, a technique based on the differential sedimentation of RNA-protein complexes after RNase treatment in density gradients. All macromolecular complexes in the cell are fractionated by a sucrose gradient followed by high-resolution proteomics. We have compared gradients of RNase-treated with untreated samples in triplicates. If a protein was part of an RNA-protein complex, the complex should be disassembled after the RNase treatment and a shift of the protein position in the gradient should be observed (RNA-dependent proteins). Our approach yielded 333 RNA-dependent proteins. The results were compared to a bioinformatic prediction of RBPs and biochemical validation. We validated in vivo the RNA-binding capacity of 6 new RBPs. Some of these proteins were previously known to be involved in essential biological processes such as photosynthesis or heterocyst differentiation, but their association with RNA was previously unknown. In other cases, the function of the validated candidates was unknown. A knock-out strain of alr1700, a gene encoding a validated RNA-binding protein of unknown function, showed a deregulation of heterocyst differentiation, confirming the role of RBPs in regulating this cell differentiation process.

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