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Direct RNA Sequencing Reveals Stress-Dependent and Pathway-Specific rRNA Modification Reprogramming during 50S

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Summary
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This study reveals how RNA modifications are regulated during ribosome assembly in E. coli. It shows that pseudouridine (Ψ) 2608 levels change depending on the assembly pathway, indicating a new layer of control in ribosome biogenesis.

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Area of Science:

  • Molecular Biology
  • Genetics
  • Biochemistry

Background:

  • Ribosome biogenesis is a complex process involving ribosomal RNA (rRNA) modification and processing.
  • Ribosomal proteins and rRNA undergo intricate assembly steps to form functional ribosomes.
  • The role of specific RNA modifications and their dynamic regulation during ribosome assembly remains an active area of research.

Purpose of the Study:

  • To investigate the impact of DbpA variants on rRNA modification patterns and 3' end processing during ribosome assembly.
  • To simultaneously detect and quantify multiple rRNA modifications in different assembly intermediates and mature subunits.
  • To explore how alternative assembly pathways influence rRNA modification incorporation.

Main Methods:

  • Oxford Nanopore direct RNA sequencing was employed for simultaneous detection and quantification of multiple RNA modifications.
  • Analysis was performed on 23S rRNA from mature 50S large subunits (LSU) and assembly intermediates (35S and 45S) in Escherichia coli.
  • Comparative analysis was conducted between cells expressing wild-type DbpA and a helicase-inactive R331A DbpA variant.

Main Results:

  • Most 23S rRNA modifications were incorporated at similar levels in intermediates and mature subunits, regardless of DbpA status, suggesting early incorporation.
  • A subset of three modifications showed altered incorporation: m2A 2507 was reduced, Ψ 2508 was increased, and Ψ 2608 was reduced in the 50S subunit from R331A DbpA cells compared to intermediates.
  • Pseudouridine (Ψ) 2608 incorporation was selectively reprogrammed across distinct in vivo assembly routes, particularly in the context of R331A DbpA expression.

Conclusions:

  • rRNA modifications are generally incorporated prior to the accumulation of major assembly intermediates and are not significantly reprogrammed under assembly stress.
  • The study identified altered incorporation patterns for specific modifications (m2A 2507, Ψ 2508, Ψ 2608) in the R331A DbpA mutant.
  • Selective reprogramming of Ψ 2608 incorporation across alternative assembly pathways reveals a novel regulatory mechanism in ribosome biogenesis.