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Common and phylogenetically widespread coding for peptides by bacterial small RNAs.

Robin C Friedman1,2,3, Stefan Kalkhof4,5, Olivia Doppelt-Azeroual6

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Bacterial small RNAs (sRNAs) frequently encode small proteins, with at least 10% having coding open reading frames (ORFs). These novel coding sRNAs are often involved in essential cellular processes and virulence.

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Machine learningMass spectrometryRibosome profilingShort ORFsType I toxin/antitoxinsRNAs

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Area of Science:

  • Microbiology
  • Genomics
  • Bioinformatics

Background:

  • Bacterial transcription is pervasive, with small RNAs (sRNAs) often assumed to be noncoding.
  • However, many sRNAs possess open reading frames (ORFs) capable of encoding small proteins, irrespective of their RNA-level regulatory roles.

Purpose of the Study:

  • To quantify the prevalence of protein-coding ORFs within bacterial sRNAs across diverse species.
  • To identify novel coding sRNAs and their potential functions using computational and experimental approaches.

Main Methods:

  • Applied machine learning techniques integrating sequence features and comparative genomics to analyze sRNA ORFs in 14 bacterial species.
  • Validated predictions using mass spectrometry proteomics and ribosome profiling data.
  • Quantified prediction uncertainty to ensure robust findings.

Main Results:

  • A majority of annotated sRNAs contain ORFs (10-50 amino acids).
  • Conservatively predicted 409±191.7 unannotated sRNA ORFs under selection for coding function (average 29 per species).
  • At least 10.3% of sRNAs possess coding ORFs; some species show up to 20%.
  • Identified novel coding ORFs, some overlapping with annotated ORFs, and many predicted as components of type I toxin/antitoxin systems.
  • Experimental validation confirmed translation of many predicted ORFs.
  • Coding sRNAs in B. subtilis are highly expressed in biofilms; in S. pneumoniae, they are linked to virulence.

Conclusions:

  • Identified over two dozen new protein-coding genes per bacterial species, with quantified uncertainty.
  • Provided accessible predictions for sRNA coding ORFs and type I toxin/antitoxin systems.
  • These findings offer valuable resources for studying bacterial sRNAs, toxin/antitoxin systems, genetics, and genomics.