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Relationship between operon preference and functional properties of persistent genes in bacterial genomes.

Bratlie MS, Johansen J, Drabløs F - BMC Genomics (2010)

Bottom Line: This indicates that there are opposing effects influencing the tendency for operon formation, and these effects may be reflected in properties like evolutionary rate, complex formation, metabolic pathways and gene fusion.Genes with a weak tendency for operon participation tend to produce proteins with more interaction partners, but possibly in more dynamic complexes and convergent pathways.Genes that are not regulated through operons are therefore more evolutionary constrained than the corresponding operon-associated genes and will on average evolve more slowly.

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Affiliation: Department of Cancer Research and Molecular Medicine, Norwegian University of Science and Technology, N-7006 Trondheim, Norway.

ABSTRACT

Background: Genes in bacteria may be organised into operons, leading to strict co-expression of the genes that participate in the same operon. However, comparisons between different bacterial genomes have shown that much of the operon structure is dynamic on an evolutionary time scale. This indicates that there are opposing effects influencing the tendency for operon formation, and these effects may be reflected in properties like evolutionary rate, complex formation, metabolic pathways and gene fusion.

Results: We have used multi-species protein-protein comparisons to generate a high-quality set of genes that are persistent in bacterial genomes (i.e. they have close to universal distribution). We have analysed these genes with respect to operon participation and important functional properties, including evolutionary rate and protein-protein interactions.

Conclusions: Genes for ribosomal proteins show a very slow rate of evolution. This is consistent with a strong tendency for the genes to participate in operons and for their proteins to be involved in essential and well defined complexes. Persistent genes for non-ribosomal proteins can be separated into two classes according to tendency to participate in operons. Those with a strong tendency for operon participation make proteins with fewer interaction partners that seem to participate in relatively static complexes and possibly linear pathways. Genes with a weak tendency for operon participation tend to produce proteins with more interaction partners, but possibly in more dynamic complexes and convergent pathways. Genes that are not regulated through operons are therefore more evolutionary constrained than the corresponding operon-associated genes and will on average evolve more slowly.

Show MeSH
Genomic range of persistent genes. Genomic range of persistent genes expressed as a percentage of genome size. The four linear genomes are marked with black points; the grey points represent circular genomes.
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Figure 2: Genomic range of persistent genes. Genomic range of persistent genes expressed as a percentage of genome size. The four linear genomes are marked with black points; the grey points represent circular genomes.

Mentions: We looked into the possibility that gene clustering might be a large scale feature with clustering of persistent genes into specific genomic regions, rather than just a local operon-based feature. In Figure 2 the genomic range spanned by persistent genes is plotted for all the 113 genomes. In circular genomes the window giving the shortest range was always selected; the procedure is further explained in Methods. The values are calculated in percentage of genome size. As the figure shows, there is a clear tendency that the persistent genes in almost every case are spread throughout most (80-100%) of the genome. However, there are some bacteria where the persistent genes cover a slightly smaller genomic range (70-80%). These bacteria are Geobacillus kaustophilus, Photobacterium profundum, Nocardia farcinica, Pseudomonas fluorescens and Streptomyces coelicolor. It is important to point out that this analysis only shows that persistent genes tend to occupy a large genomic range. Most genes may still be clustered within that range. This is further analysed below, as part of the gene cluster and operon structure. Genomic distribution of the orthologs in E. coli, the chosen model organism, is shown as a genome atlas map [36] (Figure 3), and this confirms the global distribution of persistent genes.


Relationship between operon preference and functional properties of persistent genes in bacterial genomes.

Bratlie MS, Johansen J, Drabløs F - BMC Genomics (2010)

Genomic range of persistent genes. Genomic range of persistent genes expressed as a percentage of genome size. The four linear genomes are marked with black points; the grey points represent circular genomes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2837039&req=5

Figure 2: Genomic range of persistent genes. Genomic range of persistent genes expressed as a percentage of genome size. The four linear genomes are marked with black points; the grey points represent circular genomes.
Mentions: We looked into the possibility that gene clustering might be a large scale feature with clustering of persistent genes into specific genomic regions, rather than just a local operon-based feature. In Figure 2 the genomic range spanned by persistent genes is plotted for all the 113 genomes. In circular genomes the window giving the shortest range was always selected; the procedure is further explained in Methods. The values are calculated in percentage of genome size. As the figure shows, there is a clear tendency that the persistent genes in almost every case are spread throughout most (80-100%) of the genome. However, there are some bacteria where the persistent genes cover a slightly smaller genomic range (70-80%). These bacteria are Geobacillus kaustophilus, Photobacterium profundum, Nocardia farcinica, Pseudomonas fluorescens and Streptomyces coelicolor. It is important to point out that this analysis only shows that persistent genes tend to occupy a large genomic range. Most genes may still be clustered within that range. This is further analysed below, as part of the gene cluster and operon structure. Genomic distribution of the orthologs in E. coli, the chosen model organism, is shown as a genome atlas map [36] (Figure 3), and this confirms the global distribution of persistent genes.

Bottom Line: This indicates that there are opposing effects influencing the tendency for operon formation, and these effects may be reflected in properties like evolutionary rate, complex formation, metabolic pathways and gene fusion.Genes with a weak tendency for operon participation tend to produce proteins with more interaction partners, but possibly in more dynamic complexes and convergent pathways.Genes that are not regulated through operons are therefore more evolutionary constrained than the corresponding operon-associated genes and will on average evolve more slowly.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Cancer Research and Molecular Medicine, Norwegian University of Science and Technology, N-7006 Trondheim, Norway.

ABSTRACT

Background: Genes in bacteria may be organised into operons, leading to strict co-expression of the genes that participate in the same operon. However, comparisons between different bacterial genomes have shown that much of the operon structure is dynamic on an evolutionary time scale. This indicates that there are opposing effects influencing the tendency for operon formation, and these effects may be reflected in properties like evolutionary rate, complex formation, metabolic pathways and gene fusion.

Results: We have used multi-species protein-protein comparisons to generate a high-quality set of genes that are persistent in bacterial genomes (i.e. they have close to universal distribution). We have analysed these genes with respect to operon participation and important functional properties, including evolutionary rate and protein-protein interactions.

Conclusions: Genes for ribosomal proteins show a very slow rate of evolution. This is consistent with a strong tendency for the genes to participate in operons and for their proteins to be involved in essential and well defined complexes. Persistent genes for non-ribosomal proteins can be separated into two classes according to tendency to participate in operons. Those with a strong tendency for operon participation make proteins with fewer interaction partners that seem to participate in relatively static complexes and possibly linear pathways. Genes with a weak tendency for operon participation tend to produce proteins with more interaction partners, but possibly in more dynamic complexes and convergent pathways. Genes that are not regulated through operons are therefore more evolutionary constrained than the corresponding operon-associated genes and will on average evolve more slowly.

Show MeSH