Reductive Evolution and Diversification of C5-Uracil Methylation in the Nucleic Acids of Mollicutes
Pascal Sirand-Pugnet,
Damien Brégeon,
Laure Béven,
Catherine Goyenvalle,
Alain Blanchard,
Simon Rose,
Henri Grosjean,
Stephen Douthwaite,
Djemel Hamdane,
Valérie de Crécy-Lagard
Affiliations
Pascal Sirand-Pugnet
INRAE, UMR BFP, University Bordeaux, 33882 Bordeaux Villenave D’Ornon, France
Damien Brégeon
IBPS, Biology of Aging and Adaptation, Sorbonne University, 7 quai Saint Bernard, CEDEX 05, F-75252 Paris, France
Laure Béven
INRAE, UMR BFP, University Bordeaux, 33882 Bordeaux Villenave D’Ornon, France
Catherine Goyenvalle
IBPS, Biology of Aging and Adaptation, Sorbonne University, 7 quai Saint Bernard, CEDEX 05, F-75252 Paris, France
Alain Blanchard
INRAE, UMR BFP, University Bordeaux, 33882 Bordeaux Villenave D’Ornon, France
Simon Rose
Department of Biochemistry and Molecular Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark
Henri Grosjean
Institute for Integrative Biology of the Cell (I2BC), French Atomic Energy and Energy Commission Alternatives, CNRS, Paris-Sud University, Paris-Saclay University, Gif-sur-Yvette CEDEX, 91198 Paris, France
Stephen Douthwaite
Department of Biochemistry and Molecular Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark
Djemel Hamdane
Laboratory of Biological Process Chemistry, CNRS-UMR 8229, College De France, Sorbonne University, 11 Place Marcelin Berthelot, CEDEX 05, 75231 Paris, France
Valérie de Crécy-Lagard
Department of Microbiology and Cell Science, University of Florida, Gainesville, FL 32611, USA
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 rRNA. 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.
