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Characterization of relationships between transcriptional units and operon structures in Bacillus subtilis and Escherichia coli.

Okuda S, Kawashima S, Kobayashi K, Ogasawara N, Kanehisa M, Goto S - BMC Genomics (2007)

Bottom Line: Consequently, we found that the levels of gene co-regulation was correlated to intergenic distances and gene expression levels.Most interestingly, we found that functional associations in SOPs were more observed in the environmental and genetic information processes.In addition, such differences may play an important role in the evolution of gene order across genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto 611-0011, Japan. okuda@kuicr.kyoto-u.ac.jp <okuda@kuicr.kyoto-u.ac.jp>

ABSTRACT

Background: Operon structures play an important role in transcriptional regulation in prokaryotes. However, there have been fewer studies on complicated operon structures in which the transcriptional units vary with changing environmental conditions. Information about such complicated operons is helpful for predicting and analyzing operon structures, as well as understanding gene functions and transcriptional regulation.

Results: We systematically analyzed the experimentally verified transcriptional units (TUs) in Bacillus subtilis and Escherichia coli obtained from ODB and RegulonDB. To understand the relationships between TUs and operons, we defined a new classification system for adjacent gene pairs, divided into three groups according to the level of gene co-regulation: operon pairs (OP) belong to the same TU, sub-operon pairs (SOP) that are at the transcriptional boundaries within an operon, and non-operon pairs (NOP) belonging to different operons. Consequently, we found that the levels of gene co-regulation was correlated to intergenic distances and gene expression levels. Additional analysis revealed that they were also correlated to the levels of conservation across about 200 prokaryotic genomes. Most interestingly, we found that functional associations in SOPs were more observed in the environmental and genetic information processes.

Conclusion: Complicated operon structures were correlated with genome organization and gene expression profiles. Such intricately regulated operons allow functional differences depending on environmental conditions. These regulatory mechanisms are helpful in accommodating the variety of changes that happen around the cell. In addition, such differences may play an important role in the evolution of gene order across genomes.

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Functional associations between adjacent gene pairs. The upper figures indicate the functional associations in B. subtilis and the lower represent E. coli. The proportion of gene pairs that have the functional categories shown on the x and y axis is represented by a box with red color. When the color is deeper, it indicates the proportion is increasing.
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Figure 5: Functional associations between adjacent gene pairs. The upper figures indicate the functional associations in B. subtilis and the lower represent E. coli. The proportion of gene pairs that have the functional categories shown on the x and y axis is represented by a box with red color. When the color is deeper, it indicates the proportion is increasing.

Mentions: To get a broader point of view than only the co-occurence on biological pathway maps, we measured the co-occuring frequency of these three groups of adjacent gene pairs on hierarchical categories of gene functions. We counted the number of gene pairs that shared the same category at the second level of the hierarchy (e.g. Carbohydrate metabolism). We used 22 categories that are related to prokaryotes. In Figure 5, each box represents the proportion of gene pairs that have the functional categories given on the x and y axis in B. subtilis (top) and E. coli (bottom). The deeper color indicates increasing frequency of gene pairs with the given functional categories. Additional file 1 includes the statistical analysis of these functional sharings using chi-square values. In OPs, the diagonal boxes are clearly represented by the deep red color. Statistical analysis reveals significant diagonal factors in functional sharing of OPs, even compared to Figure 5. Thus, gene pairs in OPs tend to have related functions. On the other hand, it was clear that almost all of the boxes as well as the diagonals in NOPs did not show high values. Particularly in statistical analysis they were almost similar as expected, so they did not share the related functions and can be randomly distributed. More gene pairs in SOPs were in related functional categories, compared to NOPs. In addition, gene pairs in the 'Genetic information processing' and 'Environmental information processing' groups were more likely to share functions in SOPs, compared to the other two groups. This trend was clearly shown in statistical analysis in Additional file 1. 'Transcription', 'Translation', 'Folding, Sorting and Degradation' and 'Replication and Repair' in 'Genetic information processing', and 'Membrane Transport', 'Signal Transduction' and 'Cell Growth and Death' in 'Environmental information processing' showed significant correlations. It seems to be an inherent property of SOPs that the degree of sharing between such categories and 'Metabolism' is also relatively frequent. We speculate that the functional bias of SOPs to these categories relates to the regulation of gene expression because SOPs are located on the boundary of the regulatory elements.


Characterization of relationships between transcriptional units and operon structures in Bacillus subtilis and Escherichia coli.

Okuda S, Kawashima S, Kobayashi K, Ogasawara N, Kanehisa M, Goto S - BMC Genomics (2007)

Functional associations between adjacent gene pairs. The upper figures indicate the functional associations in B. subtilis and the lower represent E. coli. The proportion of gene pairs that have the functional categories shown on the x and y axis is represented by a box with red color. When the color is deeper, it indicates the proportion is increasing.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1808063&req=5

Figure 5: Functional associations between adjacent gene pairs. The upper figures indicate the functional associations in B. subtilis and the lower represent E. coli. The proportion of gene pairs that have the functional categories shown on the x and y axis is represented by a box with red color. When the color is deeper, it indicates the proportion is increasing.
Mentions: To get a broader point of view than only the co-occurence on biological pathway maps, we measured the co-occuring frequency of these three groups of adjacent gene pairs on hierarchical categories of gene functions. We counted the number of gene pairs that shared the same category at the second level of the hierarchy (e.g. Carbohydrate metabolism). We used 22 categories that are related to prokaryotes. In Figure 5, each box represents the proportion of gene pairs that have the functional categories given on the x and y axis in B. subtilis (top) and E. coli (bottom). The deeper color indicates increasing frequency of gene pairs with the given functional categories. Additional file 1 includes the statistical analysis of these functional sharings using chi-square values. In OPs, the diagonal boxes are clearly represented by the deep red color. Statistical analysis reveals significant diagonal factors in functional sharing of OPs, even compared to Figure 5. Thus, gene pairs in OPs tend to have related functions. On the other hand, it was clear that almost all of the boxes as well as the diagonals in NOPs did not show high values. Particularly in statistical analysis they were almost similar as expected, so they did not share the related functions and can be randomly distributed. More gene pairs in SOPs were in related functional categories, compared to NOPs. In addition, gene pairs in the 'Genetic information processing' and 'Environmental information processing' groups were more likely to share functions in SOPs, compared to the other two groups. This trend was clearly shown in statistical analysis in Additional file 1. 'Transcription', 'Translation', 'Folding, Sorting and Degradation' and 'Replication and Repair' in 'Genetic information processing', and 'Membrane Transport', 'Signal Transduction' and 'Cell Growth and Death' in 'Environmental information processing' showed significant correlations. It seems to be an inherent property of SOPs that the degree of sharing between such categories and 'Metabolism' is also relatively frequent. We speculate that the functional bias of SOPs to these categories relates to the regulation of gene expression because SOPs are located on the boundary of the regulatory elements.

Bottom Line: Consequently, we found that the levels of gene co-regulation was correlated to intergenic distances and gene expression levels.Most interestingly, we found that functional associations in SOPs were more observed in the environmental and genetic information processes.In addition, such differences may play an important role in the evolution of gene order across genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Bioinformatics Center, Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto 611-0011, Japan. okuda@kuicr.kyoto-u.ac.jp <okuda@kuicr.kyoto-u.ac.jp>

ABSTRACT

Background: Operon structures play an important role in transcriptional regulation in prokaryotes. However, there have been fewer studies on complicated operon structures in which the transcriptional units vary with changing environmental conditions. Information about such complicated operons is helpful for predicting and analyzing operon structures, as well as understanding gene functions and transcriptional regulation.

Results: We systematically analyzed the experimentally verified transcriptional units (TUs) in Bacillus subtilis and Escherichia coli obtained from ODB and RegulonDB. To understand the relationships between TUs and operons, we defined a new classification system for adjacent gene pairs, divided into three groups according to the level of gene co-regulation: operon pairs (OP) belong to the same TU, sub-operon pairs (SOP) that are at the transcriptional boundaries within an operon, and non-operon pairs (NOP) belonging to different operons. Consequently, we found that the levels of gene co-regulation was correlated to intergenic distances and gene expression levels. Additional analysis revealed that they were also correlated to the levels of conservation across about 200 prokaryotic genomes. Most interestingly, we found that functional associations in SOPs were more observed in the environmental and genetic information processes.

Conclusion: Complicated operon structures were correlated with genome organization and gene expression profiles. Such intricately regulated operons allow functional differences depending on environmental conditions. These regulatory mechanisms are helpful in accommodating the variety of changes that happen around the cell. In addition, such differences may play an important role in the evolution of gene order across genomes.

Show MeSH
Related in: MedlinePlus