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Adaptation in bacterial flagellar and motility systems: from regulon members to 'foraging'-like behavior in E. coli.

Zhao K, Liu M, Burgess RR - Nucleic Acids Res. (2007)

Bottom Line: Bacterial flagellar motility and chemotaxis help cells to reach the most favorable environments and to successfully compete with other micro-organisms in response to external stimuli.To define the physiological role of these two regulators, we carried out transcription profiling experiments to identify, on a genome-wide basis, genes under the control of these two regulators.In addition, the synchronized pattern of increasing CRP activity causing increasing FlhDC expression with decreasing carbon source quality, together with the apparent coupling of motility activity with the activation of motility and chemotaxis genes in poor quality carbon sources, highlights the importance of CRP activation in allowing E. coli to devote progressively more of its limited reserves to search out better conditions.

View Article: PubMed Central - PubMed

Affiliation: McArdle Laboratory for Cancer Research, Department of Genetics, University of Wisconsin, Madison, WI 53706, USA.

ABSTRACT
Bacterial flagellar motility and chemotaxis help cells to reach the most favorable environments and to successfully compete with other micro-organisms in response to external stimuli. Escherichia coli is a motile gram-negative bacterium, and the flagellar regulon in E. coli is controlled by a master regulator FlhDC as well as a second regulator, flagellum-specific sigma factor, sigma(F). To define the physiological role of these two regulators, we carried out transcription profiling experiments to identify, on a genome-wide basis, genes under the control of these two regulators. In addition, the synchronized pattern of increasing CRP activity causing increasing FlhDC expression with decreasing carbon source quality, together with the apparent coupling of motility activity with the activation of motility and chemotaxis genes in poor quality carbon sources, highlights the importance of CRP activation in allowing E. coli to devote progressively more of its limited reserves to search out better conditions. In adaptation to a variety of carbon sources, the motile bacteria carry out tactical responses by increasing flagellar operation but restricting costly flagellar synthesis, indicating its capability of strategically using the precious energy in nutrient-poor environments for maximizing survival.

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The location and transcription direction of genes in the FlhDC and FliA regulons on the map of the E. coli genome. The outer scale point circle indicates the coordinates in minutes (100 equals intervals of DNA). Blue arrows show the locations and directions of transcription of 53 known flagellar regulon genes. Most of these genes are located in regions I, II and III (i.e. at 24, 42 and 43 min in centisomes, respectively), except three chemotaxis genes trg, aer and tsr, which are at 32, 69, 98 min, respectively. The black arrows show all the genes (117) in FlhDC regulon that were identified by our microarray studies, which include all the previously known flagellar-related genes. The pink arrows show 37 σF-dependent genes identified in our microarray studies. These include all 21 previous known σF-controlled genes in flagellar system. The origin and terminus of replication are shown as yellow lines, with black arrows indicating replichores. The next point circle in light blue gives the scale in base pairs. The inner circle shows ORFs distribution on two complement DNA strands as presented in (24).
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Figure 2: The location and transcription direction of genes in the FlhDC and FliA regulons on the map of the E. coli genome. The outer scale point circle indicates the coordinates in minutes (100 equals intervals of DNA). Blue arrows show the locations and directions of transcription of 53 known flagellar regulon genes. Most of these genes are located in regions I, II and III (i.e. at 24, 42 and 43 min in centisomes, respectively), except three chemotaxis genes trg, aer and tsr, which are at 32, 69, 98 min, respectively. The black arrows show all the genes (117) in FlhDC regulon that were identified by our microarray studies, which include all the previously known flagellar-related genes. The pink arrows show 37 σF-dependent genes identified in our microarray studies. These include all 21 previous known σF-controlled genes in flagellar system. The origin and terminus of replication are shown as yellow lines, with black arrows indicating replichores. The next point circle in light blue gives the scale in base pairs. The inner circle shows ORFs distribution on two complement DNA strands as presented in (24).

Mentions: Expression profiling of transcripts corresponding to the complete set of ORFs in the E. coli genome revealed that the response to deletion of FlhDC in vivo was quite broad. There are 117 genes (2.7% of the genome) downregulated 2-fold or more in the flhDC deletion mutant strain. The wide distribution of FlhDC-dependent genes in E. coli genome (as shown in Figure 2) indicates that FlhDC might play a larger role in the global gene transcription regulation than just to serve as a master regulator for the flagellar regulon. There are 53 genes in E. coli known to be directly involved in flagellar structure and motor function (11,12). Compared with the transcriptional level of genes in the wild-type strain, DNA microarray results showed the transcriptional level of all these genes are significantly downregulated in the FlhDC deletion strain (see Supplemental Material, Table S1). Most of these known genes in the flagellar regulon were initially identified through genetic mutagenesis analysis and can be divided into two functional groups: (1) chemotaxis and mobility; (2) surface structures.Figure 2.


Adaptation in bacterial flagellar and motility systems: from regulon members to 'foraging'-like behavior in E. coli.

Zhao K, Liu M, Burgess RR - Nucleic Acids Res. (2007)

The location and transcription direction of genes in the FlhDC and FliA regulons on the map of the E. coli genome. The outer scale point circle indicates the coordinates in minutes (100 equals intervals of DNA). Blue arrows show the locations and directions of transcription of 53 known flagellar regulon genes. Most of these genes are located in regions I, II and III (i.e. at 24, 42 and 43 min in centisomes, respectively), except three chemotaxis genes trg, aer and tsr, which are at 32, 69, 98 min, respectively. The black arrows show all the genes (117) in FlhDC regulon that were identified by our microarray studies, which include all the previously known flagellar-related genes. The pink arrows show 37 σF-dependent genes identified in our microarray studies. These include all 21 previous known σF-controlled genes in flagellar system. The origin and terminus of replication are shown as yellow lines, with black arrows indicating replichores. The next point circle in light blue gives the scale in base pairs. The inner circle shows ORFs distribution on two complement DNA strands as presented in (24).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1935009&req=5

Figure 2: The location and transcription direction of genes in the FlhDC and FliA regulons on the map of the E. coli genome. The outer scale point circle indicates the coordinates in minutes (100 equals intervals of DNA). Blue arrows show the locations and directions of transcription of 53 known flagellar regulon genes. Most of these genes are located in regions I, II and III (i.e. at 24, 42 and 43 min in centisomes, respectively), except three chemotaxis genes trg, aer and tsr, which are at 32, 69, 98 min, respectively. The black arrows show all the genes (117) in FlhDC regulon that were identified by our microarray studies, which include all the previously known flagellar-related genes. The pink arrows show 37 σF-dependent genes identified in our microarray studies. These include all 21 previous known σF-controlled genes in flagellar system. The origin and terminus of replication are shown as yellow lines, with black arrows indicating replichores. The next point circle in light blue gives the scale in base pairs. The inner circle shows ORFs distribution on two complement DNA strands as presented in (24).
Mentions: Expression profiling of transcripts corresponding to the complete set of ORFs in the E. coli genome revealed that the response to deletion of FlhDC in vivo was quite broad. There are 117 genes (2.7% of the genome) downregulated 2-fold or more in the flhDC deletion mutant strain. The wide distribution of FlhDC-dependent genes in E. coli genome (as shown in Figure 2) indicates that FlhDC might play a larger role in the global gene transcription regulation than just to serve as a master regulator for the flagellar regulon. There are 53 genes in E. coli known to be directly involved in flagellar structure and motor function (11,12). Compared with the transcriptional level of genes in the wild-type strain, DNA microarray results showed the transcriptional level of all these genes are significantly downregulated in the FlhDC deletion strain (see Supplemental Material, Table S1). Most of these known genes in the flagellar regulon were initially identified through genetic mutagenesis analysis and can be divided into two functional groups: (1) chemotaxis and mobility; (2) surface structures.Figure 2.

Bottom Line: Bacterial flagellar motility and chemotaxis help cells to reach the most favorable environments and to successfully compete with other micro-organisms in response to external stimuli.To define the physiological role of these two regulators, we carried out transcription profiling experiments to identify, on a genome-wide basis, genes under the control of these two regulators.In addition, the synchronized pattern of increasing CRP activity causing increasing FlhDC expression with decreasing carbon source quality, together with the apparent coupling of motility activity with the activation of motility and chemotaxis genes in poor quality carbon sources, highlights the importance of CRP activation in allowing E. coli to devote progressively more of its limited reserves to search out better conditions.

View Article: PubMed Central - PubMed

Affiliation: McArdle Laboratory for Cancer Research, Department of Genetics, University of Wisconsin, Madison, WI 53706, USA.

ABSTRACT
Bacterial flagellar motility and chemotaxis help cells to reach the most favorable environments and to successfully compete with other micro-organisms in response to external stimuli. Escherichia coli is a motile gram-negative bacterium, and the flagellar regulon in E. coli is controlled by a master regulator FlhDC as well as a second regulator, flagellum-specific sigma factor, sigma(F). To define the physiological role of these two regulators, we carried out transcription profiling experiments to identify, on a genome-wide basis, genes under the control of these two regulators. In addition, the synchronized pattern of increasing CRP activity causing increasing FlhDC expression with decreasing carbon source quality, together with the apparent coupling of motility activity with the activation of motility and chemotaxis genes in poor quality carbon sources, highlights the importance of CRP activation in allowing E. coli to devote progressively more of its limited reserves to search out better conditions. In adaptation to a variety of carbon sources, the motile bacteria carry out tactical responses by increasing flagellar operation but restricting costly flagellar synthesis, indicating its capability of strategically using the precious energy in nutrient-poor environments for maximizing survival.

Show MeSH
Related in: MedlinePlus