Codon usage bias and tRNA over-expression in Buchnera aphidicola after aromatic amino acid nutritional stress on its host Acyrthosiphon pisum H. Charles, F. Calevro, J. Vinuelas, J.M. Fayard, Yvan Rahbé
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H. Charles, F. Calevro, J. Vinuelas, J.M. Fayard, Yvan Rahbé. Codon usage bias and tRNA over-expression in Buchnera aphidicola after aromatic amino acid nutritional stress on its host Acyrthosiphon pisum. Nucleic Acids Research, Oxford University Press, 2006, 34 (16), pp.4583-4592. 10.1093/nar/gkl597. hal-00391277
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Distributed under a Creative Commons Attribution - NonCommercial| 4.0 International License Published online 8 September 2006 Nucleic Acids Research, 2006, Vol. 34, No. 16 4583–4592 doi:10.1093/nar/gkl597 Codon usage bias and tRNA over-expression in Buchnera aphidicola after aromatic amino acid nutritional stress on its host Acyrthosiphon pisum Hubert Charles*, Federica Calevro, Jose´ Vinuelas, Jean-Michel Fayard and Yvan Rahbe
Laboratoire de Biologie Fonctionnelle Insectes et Interactions, UMR INRA/INSA de Lyon 203, Baˆtiment Louis Pasteur, 69621 Villeurbanne Cedex, France
Received May 16, 2006; Revised July 12, 2006; Accepted August 1, 2006
ABSTRACT essential amino acids that the aphid host cannot synthesize or find in sufficient quantities in plant phloem sap (1,2). Codon usage bias and relative abundances of The Buchnera genome presents all the characteristics of tRNA isoacceptors were analysed in the obligate a vertically transmitted intracellular bacterium (3): (i) a small intracellular symbiotic bacterium, Buchnera aphidi- size of 400–600 kb, depending on host species (4); (ii) a cola from the aphid Acyrthosiphon pisum, using highly biased base composition towards A and T (5); and a dedicated 35mer oligonucleotide microarray. (iii) a high-evolutionary rate due to drastic bottlenecks and Buchnera is archetypal of organisms living with the absence of recombination, occurring in the population minimal metabolic requirements and presents a dynamics of the bacteria following transmission through reduced genome with high-evolutionary rate. Codon host generations (6). During its intracellular evolution, usage in Buchnera has been overcome by the high Buchnera has conserved most of the genes encoding vital mutational bias towards AT bases. However, several physiological functions for the symbiotic entity. As an exam- ple, enzymes of the essential amino acid biosynthesis path- lines of evidence for codon usage selection are ways were conserved whereas most of the genes encoding given here. A significant correlation was found proteins involved in non-essential amino acid biosynthesis between tRNA relative abundances and codon com- (those the aphids would produce) are deleted. DNA repli- position of Buchnera genes. A significant codon cation and repair mechanisms have been partly deleted, as usage bias was found for the choice of rare codons compared to its free-living relative Escherichia coli. The in Buchnera: C-ending codons are preferred in same observations can be made regarding the transcription highly expressed genes, whereas G-ending codons machinery (i.e. lack of many transcriptional regulators, as are avoided. This bias is not explained by GC skew well as recognizable terminator and promoter sequences). in the bacteria and might correspond to a selection Such genes and structures have been lost during the genome for perfect matching between codon–anticodon pairs shrinkage of Buchnera, probably early in the intracellular life for some essential amino acids in Buchnera pro- style of the bacteria (7,8). As generally in all bacteria, protein translation machinery teins. Nutritional stress applied to the aphid host is also highly conserved in Buchnera. Hence, Koonin (9), induced a significant overexpression of most of the based on comparative genomics, determined a ‘consensus’ tRNA isoacceptors in bacteria. Although, molecular prokaryotic gene set composed of 60 proteins, primarily regulation of the tRNA operons in Buchnera was not those involved in translation functions. Genome comparison investigated, a correlation between relative expres- between Buchnera and E.coli, using the KEGG database sion levels and organization in transcription unit (http://www.genome.jp/kegg/), reveals that all of the 55 ribo- was found in the genome of Buchnera. somal proteins, the 12 translation factors and the 21 tRNA amino-acyl transferases found in E.coli are also present in Buchnera. It is noticeable that rRNA genes are present as a single copy in Buchnera, whereas seven copies are present INTRODUCTION in E.coli. This point is generally interpreted as a property Associated with agricultural aphid pests, Buchnera aphidicola of slow-growing organisms (10,11). is one of the best-known symbiotic intracellular bacteria of The tRNA set of Buchnera is composed of 32 isoacceptors insects. Aphids rely on Buchnera to support the rapid growth and is almost minimal, being only surpassed in compactness and reproductive potential that make them such versatile and by 8 organisms of the TIGR CMR (http://www.tigr.org), all notorious pests. Buchnera furnishes some vitamins and most of them from small genome Mollicutes (Mycoplasma), and
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