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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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Overlap between the functional expression classes of Escherichia coli (columns) and Salmonella enterica serovar Typhimurium (rows). Reported is the number of orthologous gene pairs in each combination of classes. Numbers printed in bold are overlaps between classes that are significantly enriched (P value < 0.01) and those that are faded out are significantly depleted for each other (P value < 0.01).
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mst029-F4: Overlap between the functional expression classes of Escherichia coli (columns) and Salmonella enterica serovar Typhimurium (rows). Reported is the number of orthologous gene pairs in each combination of classes. Numbers printed in bold are overlaps between classes that are significantly enriched (P value < 0.01) and those that are faded out are significantly depleted for each other (P value < 0.01).

Mentions: Figure 4 visualizes the overlap in gene content of the different functional expression classes between both organisms. Each functional expression class can be found to be enriched for the genes of at least one class of the other organism, thus indicating that these clusters are in some way preserved across evolution. The S. Typhimurium genes from Scl2 and Scl4 correspond to the E. coli genes in Ecl1 and Ecl2. Indeed, both were assigned similar functional roles in the previous analysis. Both Scl2 and Ecl2 contain genes involved in key cellular processes, such as the synthesis of the cellular components, and both are enriched in essential genes. Also Ecl1 and Scl4 share many similarities: Both include genes for cell motility and are thus regulated by FlhDC in each case, and both also include genes for aerobic respiration. They also share very similar correlation profiles; a high overall correlation to the essential classes (Ecl2 and Scl2, respectively) and a strong inner correlation, which is in line with the high EC scores of Scl2 and Scl4. There is also a strong overlap between the genes of Ecl3 and Scl5. In this case, both Scl5 and Ecl3 were reported to be involved in general stress response. These two classes also display a very similar set of correlation profiles, with a high inner correlation and anticorrelated to the essential class, meaning that the set of genes in this overlap of these two classes have likely been conserved in their functionality, which is further supported by the high EC scores of Scl5. The equivalent class for the pathogen-associated Scl3 seems to be Ecl3 as almost half of the Ecl3 genes map to those of Scl3. Here, both classes seem to be enriched for transporter proteins and targets for various global regulators, such as CRP and IHF. There is a clear difference in the correlation profiles of these two classes though: where all genes of Ecl3 had high inner correlation and were clearly anticorrelated with the essential gene class, this is much less outspoken for Scl3. Furthermore, the correlation between Scl3 and Scl5, where a large segment of the other Ecl3 genes mapped to, is very low. This indicates that the genes of Scl3 have a different expression profile than those of the stress-response cluster unlike the equivalent genes in E. coli and explains the poor conservation score of the Scl3 genes and the bimodal distribution of the Ecl3 scores. The other divergent class, namely Scl1, is not only enriched for mapping to Ecl1 but also contains many genes mapping to Ecl3 (neither depleted nor enriched). The main similarity between Scl1 and Ecl1 is that they were enriched for both amino acid metabolism and vitamin biosynthesis. Although Ecl1 was strongly correlated to the essential gene class Ecl2, Scl1 is not and its expression profiles are more related with Scl3. As Scl1 represents the largest mapping to Ecl1, it accounts for the low EC score of both these classes.Fig. 4.


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)

Overlap between the functional expression classes of Escherichia coli (columns) and Salmonella enterica serovar Typhimurium (rows). Reported is the number of orthologous gene pairs in each combination of classes. Numbers printed in bold are overlaps between classes that are significantly enriched (P value < 0.01) and those that are faded out are significantly depleted for each other (P value < 0.01).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
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getmorefigures.php?uid=PMC3649669&req=5

mst029-F4: Overlap between the functional expression classes of Escherichia coli (columns) and Salmonella enterica serovar Typhimurium (rows). Reported is the number of orthologous gene pairs in each combination of classes. Numbers printed in bold are overlaps between classes that are significantly enriched (P value < 0.01) and those that are faded out are significantly depleted for each other (P value < 0.01).
Mentions: Figure 4 visualizes the overlap in gene content of the different functional expression classes between both organisms. Each functional expression class can be found to be enriched for the genes of at least one class of the other organism, thus indicating that these clusters are in some way preserved across evolution. The S. Typhimurium genes from Scl2 and Scl4 correspond to the E. coli genes in Ecl1 and Ecl2. Indeed, both were assigned similar functional roles in the previous analysis. Both Scl2 and Ecl2 contain genes involved in key cellular processes, such as the synthesis of the cellular components, and both are enriched in essential genes. Also Ecl1 and Scl4 share many similarities: Both include genes for cell motility and are thus regulated by FlhDC in each case, and both also include genes for aerobic respiration. They also share very similar correlation profiles; a high overall correlation to the essential classes (Ecl2 and Scl2, respectively) and a strong inner correlation, which is in line with the high EC scores of Scl2 and Scl4. There is also a strong overlap between the genes of Ecl3 and Scl5. In this case, both Scl5 and Ecl3 were reported to be involved in general stress response. These two classes also display a very similar set of correlation profiles, with a high inner correlation and anticorrelated to the essential class, meaning that the set of genes in this overlap of these two classes have likely been conserved in their functionality, which is further supported by the high EC scores of Scl5. The equivalent class for the pathogen-associated Scl3 seems to be Ecl3 as almost half of the Ecl3 genes map to those of Scl3. Here, both classes seem to be enriched for transporter proteins and targets for various global regulators, such as CRP and IHF. There is a clear difference in the correlation profiles of these two classes though: where all genes of Ecl3 had high inner correlation and were clearly anticorrelated with the essential gene class, this is much less outspoken for Scl3. Furthermore, the correlation between Scl3 and Scl5, where a large segment of the other Ecl3 genes mapped to, is very low. This indicates that the genes of Scl3 have a different expression profile than those of the stress-response cluster unlike the equivalent genes in E. coli and explains the poor conservation score of the Scl3 genes and the bimodal distribution of the Ecl3 scores. The other divergent class, namely Scl1, is not only enriched for mapping to Ecl1 but also contains many genes mapping to Ecl3 (neither depleted nor enriched). The main similarity between Scl1 and Ecl1 is that they were enriched for both amino acid metabolism and vitamin biosynthesis. Although Ecl1 was strongly correlated to the essential gene class Ecl2, Scl1 is not and its expression profiles are more related with Scl3. As Scl1 represents the largest mapping to Ecl1, it accounts for the low EC score of both these classes.Fig. 4.

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