Quality control of bacterial ribosome assembly by the RNA degradosome

RNA degradosomes are protein complexes that, by processing and degrading RNAs, shape the transcriptome to control gene expression. In many Gram-negative bacteria, RNA degradosomes are proteins located at the inner membrane of the bacterium. The reason for this localisation was not understood.
Using mutants that have free degradosomes in the cytoplasm, the scientists, in a paper published in the journal Plos Biologythe results of this study show that this localisation is important to preserve the quality of ribosome assembly.

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RNA maturation and degradation shape the transcriptome by generating stable molecules required for translation (rRNA and tRNA) and by facilitating the turnover of mRNAs required for post-transcriptional control of gene expression. In bacteria and in the chloroplast of plants, RNA degradosomes are multi-enzyme complexes that mature and degrade RNA. RNA degradosomes containing RNase E are attached to the inner cytoplasmic membrane in a large family of Gram-negative bacteria (β- and γ-proteobacteria). Until now, the reason for their membrane localisation was not understood.

In this study, scientists show that a mutant strain of Escherichia coli, in which the RNA degradosome is located inside the cell, accumulates 20S and 40S particles that are precursors of defective ribosome assembly. Their protein composition is abnormal and they contain precursors of RNase E-cleaved rRNAs. They concluded that the RNA degradosomes located inside the cell in the mutant strain interfere with the assembly of ribosomal subunits.

To better understand the mechanism, they showed in vitro that rRNAs contained in intact ribosomes are resistant to cleavage by RNase E, whereas protein-free rRNAs are easily degraded. This demonstrates that the compact structure of mature ribosomes protects rRNAs from degradation by RNase E.

Most rRNA operons are in close proximity in the nucleoid, suggesting the existence of a bacterial nucleolus. The first steps in bacterial ribosome assembly involve co-transcriptional folding of rRNAs and binding of ribosomal proteins (r-proteins) in the nucleoid. Multiple assembly pathways act in parallel in cooperative blocks of rRNA folding to form the structural domains of mature ribosomal subunits. Given the complexity of the ribosome assembly process, it is not surprising that defective intermediates occasionally appear.

Membrane-bound RNA degradosomes in wild-type cells are thought to control the quality of ribosome assembly after the release of nucleoid intermediates. The attachment of the RNA degradosome to the inner cytoplasmic membrane of bacteria prevents unnecessary degradation of rRNA precursors, thus explaining why this attachment is conserved in all β- and γ-proteobacteria. The identification of molecules that interfere with the attachment of the RNA degradosome to the inner cytoplasmic membrane could have applications in pharmacology and biotechnology.

© 2023 Hadjeras et al.

Figure : RNA degradosomes attached to the inner cytoplasmic membrane control the quality of ribosome assembly after the release of nucleoid intermediates.

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Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates.
Hadjeras L, Bouvier M, Canal I, Poljak L, Morin-Ogier Q, Froment C, et al.
PLoS Biology. 5 janvier 2023. DOI:https://doi.org/10.1371/journal.pbio.3001942.

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