Preprint Article Version 1 Preserved in Portico This version is not peer-reviewed

Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes

Pascal Sirand-Pugnet
* ORCID logo ,
Damien Brégeon
,
Laure Beven
,
Catherine Goyenvalle
,
Alain Blanchard
ORCID logo ,
Simon Rose
,
Henri Grosjean
,
Stephen Douthwaite
ORCID logo ,
Djemel Hamdane
* ORCID logo ,
Valérie de Crécy-Lagard
* ORCID logo
Version 1 : Received: 6 March 2020 / Approved: 6 March 2020 / Online: 6 March 2020 (02:28:12 CET)

A peer-reviewed article of this Preprint also exists.

Sirand-Pugnet, P.; Brégeon, D.; Béven, L.; Goyenvalle, C.; Blanchard, A.; Rose, S.; Grosjean, H.; Douthwaite, S.; Hamdane, D.; Crécy-Lagard, V. Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes. Biomolecules 2020, 10, 587. Sirand-Pugnet, P.; Brégeon, D.; Béven, L.; Goyenvalle, C.; Blanchard, A.; Rose, S.; Grosjean, H.; Douthwaite, S.; Hamdane, D.; Crécy-Lagard, V. Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes. Biomolecules 2020, 10, 587.

Abstract

The C5-methylation of uracil to form 5-methyluracil (m5U) is a ubiquitous base modification of nucleic acids. Four enzyme families have converged to catalyze this methylation using different chemical solutions. Here, we investigate the evolution of 5-methyluracil synthase families in Mollicutes, a class of bacteria that has undergone extensive genome erosion. Many mollicutes have lost some of the m5U methyltransferases present in their common ancestor. Cases of duplication and subsequent shift of function are also described. For example, most members of the Spiroplasma subgroup, use the ancestral tetrahydrofolate-dependent TrmFO enzyme, to catalyze the formation of m5U54 in tRNA, while a TrmFO paralog (termed RlmFO) is responsible for m5U1939 formation in 23S RNA. RlmFO has replaced the S-adenosyl-l-methionine (SAM)-enzyme RlmD that adds the same modification in the ancestor and which is still present in mollicutes from the Hominis subgroup. Another paralog of this family, the TrmFO-like protein, has a yet unidentified function that differs from the TrmFO and RlmFO homologs. Despite having evolved towards minimal genomes, the mollicutes possess a repertoire of m5U modifying enzymes that is highly dynamic and has undergone horizontal transfer. This emphasizes the necessity for combining bioinformatics predictions with empirical testing and structural information to get a reliable functional annotation of these enzymes.

Keywords

base modification; methyltransferases; flavoenzymes; tRNA; rRNA; mycoplasmas; spiroplasmas; acholeplasmas; evolution; minimal cell; moonlighting function

Subject

Biology and Life Sciences, Immunology and Microbiology

Copyright: This is an open access article distributed under the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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