Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates.
RNA processing and degradation shape the transcriptome by generating stable molecules that are necessary for translation (rRNA and tRNA) and by facilitating the turnover of mRNA, which is necessary for the posttranscriptional control of gene expression. In bacteria and the plant chloroplast, RNA deg...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-01-01
|
| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3001942 |
| _version_ | 1828004513565376512 |
|---|---|
| author | Lydia Hadjeras Marie Bouvier Isabelle Canal Leonora Poljak Quentin Morin-Ogier Carine Froment Odile Burlet-Schlitz Lina Hamouche Laurence Girbal Muriel Cocaign-Bousquet Agamemnon J Carpousis |
| author_facet | Lydia Hadjeras Marie Bouvier Isabelle Canal Leonora Poljak Quentin Morin-Ogier Carine Froment Odile Burlet-Schlitz Lina Hamouche Laurence Girbal Muriel Cocaign-Bousquet Agamemnon J Carpousis |
| author_sort | Lydia Hadjeras |
| collection | DOAJ |
| description | RNA processing and degradation shape the transcriptome by generating stable molecules that are necessary for translation (rRNA and tRNA) and by facilitating the turnover of mRNA, which is necessary for the posttranscriptional control of gene expression. In bacteria and the plant chloroplast, RNA degradosomes are multienzyme complexes that process and degrade RNA. In many bacterial species, the endoribonuclease RNase E is the central component of the RNA degradosome. RNase E-based RNA degradosomes are inner membrane proteins in a large family of gram-negative bacteria (β- and γ-Proteobacteria). Until now, the reason for membrane localization was not understood. Here, we show that a mutant strain of Escherichia coli, in which the RNA degradosome is localized to the interior of the cell, has high levels of 20S and 40S particles that are defective intermediates in ribosome assembly. These particles have aberrant protein composition and contain rRNA precursors that have been cleaved by RNase E. After RNase E cleavage, rRNA fragments are degraded to nucleotides by exoribonucleases. In vitro, rRNA in intact ribosomes is resistant to RNase E cleavage, whereas protein-free rRNA is readily degraded. We conclude that RNA degradosomes in the nucleoid of the mutant strain interfere with cotranscriptional ribosome assembly. We propose that membrane-attached RNA degradosomes in wild-type cells control the quality of ribosome assembly after intermediates are released from the nucleoid. That is, the compact structure of mature ribosomes protects rRNA against cleavage by RNase E. Turnover of a proportion of intermediates in ribosome assembly explains slow growth of the mutant strain. Competition between mRNA and rRNA degradation could be the cause of slower mRNA degradation in the mutant strain. We conclude that attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA precursors, thus explaining the reason for conservation of membrane-attached RNA degradosomes throughout the β- and γ-Proteobacteria. |
| first_indexed | 2024-04-10T07:17:08Z |
| format | Article |
| id | doaj.art-3e65891bf00f4059945dafbd6e7a7916 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-04-10T07:17:08Z |
| publishDate | 2023-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-3e65891bf00f4059945dafbd6e7a79162023-02-25T05:30:57ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-01-01211e300194210.1371/journal.pbio.3001942Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates.Lydia HadjerasMarie BouvierIsabelle CanalLeonora PoljakQuentin Morin-OgierCarine FromentOdile Burlet-SchlitzLina HamoucheLaurence GirbalMuriel Cocaign-BousquetAgamemnon J CarpousisRNA processing and degradation shape the transcriptome by generating stable molecules that are necessary for translation (rRNA and tRNA) and by facilitating the turnover of mRNA, which is necessary for the posttranscriptional control of gene expression. In bacteria and the plant chloroplast, RNA degradosomes are multienzyme complexes that process and degrade RNA. In many bacterial species, the endoribonuclease RNase E is the central component of the RNA degradosome. RNase E-based RNA degradosomes are inner membrane proteins in a large family of gram-negative bacteria (β- and γ-Proteobacteria). Until now, the reason for membrane localization was not understood. Here, we show that a mutant strain of Escherichia coli, in which the RNA degradosome is localized to the interior of the cell, has high levels of 20S and 40S particles that are defective intermediates in ribosome assembly. These particles have aberrant protein composition and contain rRNA precursors that have been cleaved by RNase E. After RNase E cleavage, rRNA fragments are degraded to nucleotides by exoribonucleases. In vitro, rRNA in intact ribosomes is resistant to RNase E cleavage, whereas protein-free rRNA is readily degraded. We conclude that RNA degradosomes in the nucleoid of the mutant strain interfere with cotranscriptional ribosome assembly. We propose that membrane-attached RNA degradosomes in wild-type cells control the quality of ribosome assembly after intermediates are released from the nucleoid. That is, the compact structure of mature ribosomes protects rRNA against cleavage by RNase E. Turnover of a proportion of intermediates in ribosome assembly explains slow growth of the mutant strain. Competition between mRNA and rRNA degradation could be the cause of slower mRNA degradation in the mutant strain. We conclude that attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA precursors, thus explaining the reason for conservation of membrane-attached RNA degradosomes throughout the β- and γ-Proteobacteria.https://doi.org/10.1371/journal.pbio.3001942 |
| spellingShingle | Lydia Hadjeras Marie Bouvier Isabelle Canal Leonora Poljak Quentin Morin-Ogier Carine Froment Odile Burlet-Schlitz Lina Hamouche Laurence Girbal Muriel Cocaign-Bousquet Agamemnon J Carpousis Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates. PLoS Biology |
| title | Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates. |
| title_full | Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates. |
| title_fullStr | Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates. |
| title_full_unstemmed | Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates. |
| title_short | Attachment of the RNA degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rRNA in ribosome assembly intermediates. |
| title_sort | attachment of the rna degradosome to the bacterial inner cytoplasmic membrane prevents wasteful degradation of rrna in ribosome assembly intermediates |
| url | https://doi.org/10.1371/journal.pbio.3001942 |
| work_keys_str_mv | AT lydiahadjeras attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT mariebouvier attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT isabellecanal attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT leonorapoljak attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT quentinmorinogier attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT carinefroment attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT odileburletschlitz attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT linahamouche attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT laurencegirbal attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT murielcocaignbousquet attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates AT agamemnonjcarpousis attachmentofthernadegradosometothebacterialinnercytoplasmicmembranepreventswastefuldegradationofrrnainribosomeassemblyintermediates |