Conservation of the links between gene transcription and chromosomal organization in the highly reduced genome of Buchnera aphidicola

BackgroundGenomic studies on bacteria have clearly shown the existence of chromosomal organization as regards, for example, to gene localization, order and orientation. Moreover, transcriptomic analyses have demonstrated that, in free-living bacteria, gene transcription levels and chromosomal organization are mutually influenced. We have explored the possible conservation of relationships between mRNA abundances and chromosomal organization in the highly reduced genome of Buchnera aphidicola, the primary endosymbiont of the aphids, and a close relative to Escherichia coli.ResultsUsing an oligonucleotide-based microarray, we normalized the transcriptomic data by genomic DNA signals in order to have access to inter-gene comparison data. Our analysis showed that mRNA abundances, gene organization (operon) and gene essentiality are correlated in Buchnera (i.e., the most expressed genes are essential genes organized in operons) whereas no link between mRNA abundances and gene strand bias was found. The effect of Buchnera genome evolution on gene expression levels has also been analysed in order to assess the constraints imposed by the obligate symbiosis with aphids, underlining the importance of some gene sets for the survival of the two partners. Finally, our results show the existence of spatial periodic transcriptional patterns in the genome of Buchnera.ConclusionDespite an important reduction in its genome size and an apparent decay of its capacity for regulating transcription, this work reveals a significant correlation between mRNA abundances and chromosomal organization of the aphid-symbiont Buchnera.

[1]  Andrés Moya,et al.  Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[2]  E. Rocha Is there a role for replication fork asymmetry in the distribution of genes in bacterial genomes? , 2002, Trends in microbiology.

[3]  M. Hattori,et al.  Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS , 2000, Nature.

[4]  S. Mirkin,et al.  Mechanisms of Transcription-Replication Collisions in Bacteria , 2005, Molecular and Cellular Biology.

[5]  Javier Arsuaga,et al.  Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli , 2004, Genome Biology.

[6]  P. Bork,et al.  Analysis of genomic context: prediction of functional associations from conserved bidirectionally transcribed gene pairs , 2004, Nature Biotechnology.

[7]  M. Gerstein,et al.  Relationship between gene co-expression and probe localization on microarray slides , 2003, BMC Genomics.

[8]  François Képès,et al.  Transcription/replication collisions cause bacterial transcription units to be longer on the leading strand of replication , 2004, Bioinform..

[9]  Federica Calevro,et al.  Different Levels of Transcriptional Regulation Due to Trophic Constraints in the Reduced Genome of Buchnera aphidicola APS , 2006, Applied and Environmental Microbiology.

[10]  N. Moran,et al.  50 Million Years of Genomic Stasis in Endosymbiotic Bacteria , 2002, Science.

[11]  B. J. Brewer,et al.  When polymerases collide: Replication and the transcriptional organization of the E. coli chromosome , 1988, Cell.

[12]  Bernhard O. Palsson,et al.  Long-Range Periodic Patterns in Microbial Genomes Indicate Significant Multi-Scale Chromosomal Organization , 2006, PLoS Comput. Biol..

[13]  J. Fayard,et al.  Codon usage bias and tRNA over-expression in Buchnera aphidicola after aromatic amino acid nutritional stress on its host Acyrthosiphon pisum , 2006, Nucleic acids research.

[14]  Andrés Moya,et al.  A Small Microbial Genome: The End of a Long Symbiotic Relationship? , 2006, Science.

[15]  A. Moya,et al.  Gene expression levels influence amino acid usage and evolutionary rates in endosymbiotic bacteria. , 2005, Gene.

[16]  Alfonso Valencia,et al.  Reductive genome evolution in Buchnera aphidicola , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  A. Moya,et al.  Determination of the Core of a Minimal Bacterial Gene Set , 2004, Microbiology and Molecular Biology Reviews.

[18]  J. Fayard,et al.  Assessment of 35mer amino-modified oligonucleotide based microarray with bacterial samples. , 2004, Journal of microbiological methods.

[19]  Martin J Lercher,et al.  Co-expressed yeast genes cluster over a long range but are not regularly spaced. , 2006, Journal of molecular biology.

[20]  W. Hale,et al.  Genomic DNA standards for gene expression profiling in Mycobacterium tuberculosis. , 2002, Nucleic acids research.

[21]  Yukiko Yamazaki,et al.  Profiling of Escherichia coli Chromosome database. , 2008, Methods in molecular biology.

[22]  Bruno Torrésani,et al.  Decoding the nucleoid organisation of Bacillus subtilis and Escherichia coli through gene expression data , 2005, BMC Genomics.

[23]  S. Shigenobu,et al.  An experimental validation of orphan genes of Buchnera, a symbiont of aphids. , 2002, Biochemical and biophysical research communications.

[24]  E. Koonin,et al.  Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. , 2002, Genome research.

[25]  Arkady B Khodursky,et al.  Spatial patterns of transcriptional activity in the chromosome of Escherichia coli , 2004, Genome Biology.

[26]  S. French,et al.  Consequences of replication fork movement through transcription units in vivo. , 1992, Science.

[27]  Adam P. Arkin,et al.  Interruptions in gene expression drive highly expressed operons to the leading strand of DNA replication , 2005, Nucleic acids research.

[28]  H. Charles,et al.  Physical and Genetic Map of the Genome of Buchnera, the Primary Endosymbiont of the Pea Aphid Acyrthosiphon pisum , 1999, Journal of Molecular Evolution.

[29]  Eduardo P C Rocha,et al.  Gene essentiality determines chromosome organisation in bacteria. , 2003, Nucleic acids research.

[30]  Albert-László Barabási,et al.  Spurious spatial periodicity of co-expression in microarray data due to printing design. , 2003, Nucleic acids research.

[31]  S. Shigenobu,et al.  Hundreds of Flagellar Basal Bodies Cover the Cell Surface of the Endosymbiotic Bacterium Buchnera aphidicola sp. Strain APS , 2006, Journal of bacteriology.

[32]  A. Moya,et al.  Tempo and mode of early gene loss in endosymbiotic bacteria from insects , 2006, BMC Evolutionary Biology.

[33]  Benjamin Audit,et al.  From genes to genomes: universal scale-invariant properties of microbial chromosome organisation. , 2003, Journal of molecular biology.

[34]  J. Lawrence,et al.  Gene organization: selection, selfishness, and serendipity. , 2003, Annual review of microbiology.

[35]  Eduardo P C Rocha,et al.  The replication-related organization of bacterial genomes. , 2004, Microbiology.

[36]  Angela E. Douglas,et al.  The Nutritional Physiology of Aphids , 2003 .

[37]  Eduardo P C Rocha,et al.  Essentiality, not expressiveness, drives gene-strand bias in bacteria , 2003, Nature Genetics.

[38]  J Quackenbush,et al.  Use of RNA and genomic DNA references for inferred comparisons in DNA microarray analyses. , 2002, BioTechniques.

[39]  Laurent Duret,et al.  ROSO: optimizing oligonucleotide probes for microarrays , 2004, Bioinform..

[40]  N. W. Davis,et al.  The complete genome sequence of Escherichia coli K-12. , 1997, Science.

[41]  N. Moran,et al.  The process of genome shrinkage in the obligate symbiont Buchnera aphidicola , 2001, Genome Biology.

[42]  François Képès,et al.  Periodic transcriptional organization of the E.coli genome. , 2004, Journal of molecular biology.

[43]  H. Garner,et al.  Toward a universal standard: comparing two methods for standardizing spotted microarray data. , 2002, BioTechniques.