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Expression divergence between Escherichia coli and Salmonella enterica serovar Typhimurium reflects their lifestyles.

Meysman P, Sánchez-Rodríguez A, Fu Q, Marchal K, Engelen K - Mol. Biol. Evol. (2013)

Bottom Line: We found that gene expression conservation occurs mostly independently from amino acid similarity.Typhimurium.Genes involved with key cellular processes are most likely to have conserved their expression domains, whereas genes showing diverged expression are associated with metabolic processes that, although present in both species, are regulated differently.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbial and Molecular Systems, KU Leuven, Leuven, Belgium.

ABSTRACT
Escherichia coli K12 is a commensal bacteria and one of the best-studied model organisms. Salmonella enterica serovar Typhimurium, on the other hand, is a facultative intracellular pathogen. These two prokaryotic species can be considered related phylogenetically, and they share a large amount of their genetic material, which is commonly termed the "core genome." Despite their shared core genome, both species display very different lifestyles, and it is unclear to what extent the core genome, apart from the species-specific genes, plays a role in this lifestyle divergence. In this study, we focus on the differences in expression domains for the orthologous genes in E. coli and S. Typhimurium. The iterative comparison of coexpression methodology was used on large expression compendia of both species to uncover the conservation and divergence of gene expression. We found that gene expression conservation occurs mostly independently from amino acid similarity. According to our estimates, at least more than one quarter of the orthologous genes has a different expression domain in E. coli than in S. Typhimurium. Genes involved with key cellular processes are most likely to have conserved their expression domains, whereas genes showing diverged expression are associated with metabolic processes that, although present in both species, are regulated differently. The expression domains of the shared "core" genome of E. coli and S. Typhimurium, consisting of highly conserved orthologs, have been tuned to help accommodate the differences in lifestyle and the pathogenic potential of Salmonella.

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Distribution of the EC score between the orthologous genes of Escherichia coli and Salmonella enterica serovar Typhimurium depicted by its kernel smoothed density estimate (blue line). The distribution of the EC scores for gene pairs with randomized expression values, which represent the estimated score given no conservation of expression, is shown as a red line. The distribution of the EC scores resulting from comparison of the E. coli compendium to itself with data from different experiments is shown as a green line and represents the estimated score given perfect conservation of expression.
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mst029-F1: Distribution of the EC score between the orthologous genes of Escherichia coli and Salmonella enterica serovar Typhimurium depicted by its kernel smoothed density estimate (blue line). The distribution of the EC scores for gene pairs with randomized expression values, which represent the estimated score given no conservation of expression, is shown as a red line. The distribution of the EC scores resulting from comparison of the E. coli compendium to itself with data from different experiments is shown as a green line and represents the estimated score given perfect conservation of expression.

Mentions: The distribution of the EC scores of the orthologous gene pairs is given in figure 1. The distribution consists of two peaks (or “modes"), one at 0.3 and a smaller one at 0.6. There are also several gene pairs whose EC score is negative, indicating orthologs whose expression domains tend to be reversed in these two compendia. The full listing of the orthologous genes and their scores can be found in supplementary data set S1, Supplementary Material online. To facilitate comparison between the EC scores, we quantified the level of variability that can arise when the conservation and divergence is known. To this end, we constructed background distributions both for the case of expression divergence and for the case of perfect EC. The divergence background distribution is shown in figure 1. As can be seen, the EC scores of gene pairs with permutated expression values vary between −0.6 and 0.7. Additionally, we also created a background distribution for the case of conserved gene expression domains by splitting the largest expression compendium, namely E. coli, into two equal halves (multiple times), with each half containing a different set of microarray experiments. The two E. coli compendia are then compared against each other (fig. 1). In effect, we are simulating perfect conservation by comparing a species to itself but accounting for the presence of different experimental setups and conditions in both expression compendia. Surprisingly, the correlation score of a perfectly conserved gene pair can vary between −0.5 and 1. The fact that the score can be so low, even when expression should be perfectly conserved, can be attributed to the condition dependency of the EC score. Indeed, when cross-comparing the split compendium where the experimental conditions are similar in either half, the resulting EC scores are much higher (see supplementary material S2, Supplementary Material online). Although the EC score was specifically developed to compare expression compendia that do not necessarily survey the same biological conditions, a different set of conditions does affect the observed correlations between genes of the same species and hence also the EC scores.Fig. 1.


Expression divergence between Escherichia coli and Salmonella enterica serovar Typhimurium reflects their lifestyles.

Meysman P, Sánchez-Rodríguez A, Fu Q, Marchal K, Engelen K - Mol. Biol. Evol. (2013)

Distribution of the EC score between the orthologous genes of Escherichia coli and Salmonella enterica serovar Typhimurium depicted by its kernel smoothed density estimate (blue line). The distribution of the EC scores for gene pairs with randomized expression values, which represent the estimated score given no conservation of expression, is shown as a red line. The distribution of the EC scores resulting from comparison of the E. coli compendium to itself with data from different experiments is shown as a green line and represents the estimated score given perfect conservation of expression.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3649669&req=5

mst029-F1: Distribution of the EC score between the orthologous genes of Escherichia coli and Salmonella enterica serovar Typhimurium depicted by its kernel smoothed density estimate (blue line). The distribution of the EC scores for gene pairs with randomized expression values, which represent the estimated score given no conservation of expression, is shown as a red line. The distribution of the EC scores resulting from comparison of the E. coli compendium to itself with data from different experiments is shown as a green line and represents the estimated score given perfect conservation of expression.
Mentions: The distribution of the EC scores of the orthologous gene pairs is given in figure 1. The distribution consists of two peaks (or “modes"), one at 0.3 and a smaller one at 0.6. There are also several gene pairs whose EC score is negative, indicating orthologs whose expression domains tend to be reversed in these two compendia. The full listing of the orthologous genes and their scores can be found in supplementary data set S1, Supplementary Material online. To facilitate comparison between the EC scores, we quantified the level of variability that can arise when the conservation and divergence is known. To this end, we constructed background distributions both for the case of expression divergence and for the case of perfect EC. The divergence background distribution is shown in figure 1. As can be seen, the EC scores of gene pairs with permutated expression values vary between −0.6 and 0.7. Additionally, we also created a background distribution for the case of conserved gene expression domains by splitting the largest expression compendium, namely E. coli, into two equal halves (multiple times), with each half containing a different set of microarray experiments. The two E. coli compendia are then compared against each other (fig. 1). In effect, we are simulating perfect conservation by comparing a species to itself but accounting for the presence of different experimental setups and conditions in both expression compendia. Surprisingly, the correlation score of a perfectly conserved gene pair can vary between −0.5 and 1. The fact that the score can be so low, even when expression should be perfectly conserved, can be attributed to the condition dependency of the EC score. Indeed, when cross-comparing the split compendium where the experimental conditions are similar in either half, the resulting EC scores are much higher (see supplementary material S2, Supplementary Material online). Although the EC score was specifically developed to compare expression compendia that do not necessarily survey the same biological conditions, a different set of conditions does affect the observed correlations between genes of the same species and hence also the EC scores.Fig. 1.

Bottom Line: We found that gene expression conservation occurs mostly independently from amino acid similarity.Typhimurium.Genes involved with key cellular processes are most likely to have conserved their expression domains, whereas genes showing diverged expression are associated with metabolic processes that, although present in both species, are regulated differently.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbial and Molecular Systems, KU Leuven, Leuven, Belgium.

ABSTRACT
Escherichia coli K12 is a commensal bacteria and one of the best-studied model organisms. Salmonella enterica serovar Typhimurium, on the other hand, is a facultative intracellular pathogen. These two prokaryotic species can be considered related phylogenetically, and they share a large amount of their genetic material, which is commonly termed the "core genome." Despite their shared core genome, both species display very different lifestyles, and it is unclear to what extent the core genome, apart from the species-specific genes, plays a role in this lifestyle divergence. In this study, we focus on the differences in expression domains for the orthologous genes in E. coli and S. Typhimurium. The iterative comparison of coexpression methodology was used on large expression compendia of both species to uncover the conservation and divergence of gene expression. We found that gene expression conservation occurs mostly independently from amino acid similarity. According to our estimates, at least more than one quarter of the orthologous genes has a different expression domain in E. coli than in S. Typhimurium. Genes involved with key cellular processes are most likely to have conserved their expression domains, whereas genes showing diverged expression are associated with metabolic processes that, although present in both species, are regulated differently. The expression domains of the shared "core" genome of E. coli and S. Typhimurium, consisting of highly conserved orthologs, have been tuned to help accommodate the differences in lifestyle and the pathogenic potential of Salmonella.

Show MeSH
Related in: MedlinePlus