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PLoS Genet. 2014 May 8;10(5):e1004363. doi: 10.1371/journal.pgen.1004363. eCollection 2014.

Predicting the minimal translation apparatus: lessons from the reductive evolution of mollicutes.

Author information

  • 1Centre de Génétique Moléculaire, UPR 3404, CNRS, Université Paris-Sud, FRC 3115, Gif-sur-Yvette, France.
  • 2INRA, UMR 1332 de Biologie du Fruit et Pathologie, Villenave d'Ornon, France; Univ. Bordeaux, UMR 1332 de Biologie du Fruit et Pathologie, Villenave d'Ornon, France.
  • 3Anses, Laboratoire de Lyon, UMR Mycoplasmoses des Ruminants, Lyon, France; Université de Lyon, VetAgro Sup, UMR Mycoplasmoses des Ruminants, Marcy L'Etoile, France.
  • 4Centre International de Recherche en Agronomie pour le Développement, UMR CMAEE, Montpellier, France.
  • 5INRA, UMR1225, Ecole Nationale Vétérinaire de Toulouse, Toulouse, France; Université de Toulouse, INP-ENVT, UMR1225, Ecole Nationale Vétérinaire de Toulouse, Toulouse, France.
  • 6Univ. Bordeaux, Centre de bioinformatique et de génomique fonctionnelle, CBiB, Bordeaux, France.
  • 7Department of Microbiology and Cell Science, University Florida, Gainesville, Florida, United States of America.

Abstract

Mollicutes is a class of parasitic bacteria that have evolved from a common Firmicutes ancestor mostly by massive genome reduction. With genomes under 1 Mbp in size, most Mollicutes species retain the capacity to replicate and grow autonomously. The major goal of this work was to identify the minimal set of proteins that can sustain ribosome biogenesis and translation of the genetic code in these bacteria. Using the experimentally validated genes from the model bacteria Escherichia coli and Bacillus subtilis as input, genes encoding proteins of the core translation machinery were predicted in 39 distinct Mollicutes species, 33 of which are culturable. The set of 260 input genes encodes proteins involved in ribosome biogenesis, tRNA maturation and aminoacylation, as well as proteins cofactors required for mRNA translation and RNA decay. A core set of 104 of these proteins is found in all species analyzed. Genes encoding proteins involved in post-translational modifications of ribosomal proteins and translation cofactors, post-transcriptional modifications of t+rRNA, in ribosome assembly and RNA degradation are the most frequently lost. As expected, genes coding for aminoacyl-tRNA synthetases, ribosomal proteins and initiation, elongation and termination factors are the most persistent (i.e. conserved in a majority of genomes). Enzymes introducing nucleotides modifications in the anticodon loop of tRNA, in helix 44 of 16S rRNA and in helices 69 and 80 of 23S rRNA, all essential for decoding and facilitating peptidyl transfer, are maintained in all species. Reconstruction of genome evolution in Mollicutes revealed that, beside many gene losses, occasional gains by horizontal gene transfer also occurred. This analysis not only showed that slightly different solutions for preserving a functional, albeit minimal, protein synthetizing machinery have emerged in these successive rounds of reductive evolution but also has broad implications in guiding the reconstruction of a minimal cell by synthetic biology approaches.

PMID:
24809820
[PubMed - in process]
PMCID:
PMC4014445
Free PMC Article

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