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Gene regulation by H-NS as a function of growth conditions depends on chromosomal position in Escherichia coli.

Brambilla E, Sclavi B - G3 (Bethesda) (2015)

Bottom Line: Cellular adaptation to changing environmental conditions requires the coordinated regulation of expression of large sets of genes by global regulatory factors such as nucleoid associated proteins.Our results show that the activity of the Phns promoter depends on whether it is placed within the AT-rich regions of the genome that are known to be bound preferentially by H-NS.Genomic position can thus play a significant role in the adaptation of the cells to environmental changes, providing a fitness advantage that can explain the selection of a gene's position during evolution.

View Article: PubMed Central - PubMed

Affiliation: LBPA, UMR 8113 du CNRS, Ecole Normale Supérieure de Cachan, Cachan, France School of Engineering and Science, Jacobs University Bremen, Bremen, Germany.

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(A) Global view of H-NS binding, AT content, and presence of tsEPODs in the E. coli chromosome. From the bottom to the top: The macrodomains, as defined by Boccard (Valens et al. 2004). Sites bound by H-NS in early exponential (HNS_EE), mid exponential (HNS_ME), transition to stationary (HNS_TS), and stationary phase (HNS_S) (Kahramanoglou et al. 2011). There is an increase in the number and the length of regions bound by H-NS when approaching stationary phase, especially in the terminus. tsEPODs mapped on the E. coli chromosome (Vora et al. 2009). The plot shows the number of genes overlapping with tsEPODs as determined from the NUST software, with multiple sliding windows histogram performed choosing a bin number equal to 32 (Scolari et al. 2012). The AT content is calculated with a sliding window of 50 kb with a shift of 10 kb. The two horizontal dashed lines correspond to 45 and 55% AT. The terminus shows greater AT-content. H-NS binding: sites bound by H-NS in the different growth phases (Kahramanoglou et al. 2011). (B−G) Genomic neighborhood of the chromosomal insertion positions of the reporter construct. From the bottom to the top of each plot: Genes on the lagging and on the leading strand. In gray, the two convergent genes between which the Phns-yfp construct was inserted. The site of insertion is shown by a red dot. Position of the sites bound by FIS in early exponential (FIS_EE) and in mid exponential (FIS_ME) phases (Kahramanoglou et al. 2011). There are more sites bound by FIS near the origin (LO and RO, plots on the top) than in the terminus (LT and RT, plots in the bottom). Position of the sites bound by H-NS in early exponential (HNS_EE), mid exponential (HNS_ME), transition to stationary (HNS_TS) and stationary (HNS_S) phases (Kahramanoglou et al. 2011). In the proximity of LT and RO there is an extended region of sites bound by H-NS. Presence of genes identified as transcriptionally silent (Vora et al. 2009). The AT content is calculated with a 4000-bp sliding window with a shift of 500 bases. The two horizontal dashed lines correspond to 45 and 55% AT. A peak in AT-content is visible near LT and RO. FIS, factor for inversion stimulation; H-NS, histone-like nucleoid-structuring protein; LM, left medium; LO, left origin; LT, left terminus; RM, right medium; RO, right origin; RT, right terminus; tsEPODs, transcriptionally silent extended protein occupancy domains.
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fig6: (A) Global view of H-NS binding, AT content, and presence of tsEPODs in the E. coli chromosome. From the bottom to the top: The macrodomains, as defined by Boccard (Valens et al. 2004). Sites bound by H-NS in early exponential (HNS_EE), mid exponential (HNS_ME), transition to stationary (HNS_TS), and stationary phase (HNS_S) (Kahramanoglou et al. 2011). There is an increase in the number and the length of regions bound by H-NS when approaching stationary phase, especially in the terminus. tsEPODs mapped on the E. coli chromosome (Vora et al. 2009). The plot shows the number of genes overlapping with tsEPODs as determined from the NUST software, with multiple sliding windows histogram performed choosing a bin number equal to 32 (Scolari et al. 2012). The AT content is calculated with a sliding window of 50 kb with a shift of 10 kb. The two horizontal dashed lines correspond to 45 and 55% AT. The terminus shows greater AT-content. H-NS binding: sites bound by H-NS in the different growth phases (Kahramanoglou et al. 2011). (B−G) Genomic neighborhood of the chromosomal insertion positions of the reporter construct. From the bottom to the top of each plot: Genes on the lagging and on the leading strand. In gray, the two convergent genes between which the Phns-yfp construct was inserted. The site of insertion is shown by a red dot. Position of the sites bound by FIS in early exponential (FIS_EE) and in mid exponential (FIS_ME) phases (Kahramanoglou et al. 2011). There are more sites bound by FIS near the origin (LO and RO, plots on the top) than in the terminus (LT and RT, plots in the bottom). Position of the sites bound by H-NS in early exponential (HNS_EE), mid exponential (HNS_ME), transition to stationary (HNS_TS) and stationary (HNS_S) phases (Kahramanoglou et al. 2011). In the proximity of LT and RO there is an extended region of sites bound by H-NS. Presence of genes identified as transcriptionally silent (Vora et al. 2009). The AT content is calculated with a 4000-bp sliding window with a shift of 500 bases. The two horizontal dashed lines correspond to 45 and 55% AT. A peak in AT-content is visible near LT and RO. FIS, factor for inversion stimulation; H-NS, histone-like nucleoid-structuring protein; LM, left medium; LO, left origin; LT, left terminus; RM, right medium; RO, right origin; RT, right terminus; tsEPODs, transcriptionally silent extended protein occupancy domains.

Mentions: The activity of the Phns promoter depends on the activation by the FIS protein in early exponential phase at fast growth (Falconi et al. 1996), Cold shock protein A (CspA) for induction upon cold shock (La Teana et al. 1991), and on the binding of the H-NS protein itself resulting in repression (Ueguchi et al. 1993; Falconi et al. 1993). Binding of the H-NS protein along the genome is not uniform and changes as a function of the growth phase (Kahramanoglou et al. 2011; Zarei et al. 2013). When the sites of insertion of the reporter construct are mapped on the H-NS binding patterns one can see that those sites that are less expressed (LT and RO) are found in regions with a greater probability of H-NS binding as measured by formaldehyde crosslinking (Figure 6 and Figure S4).


Gene regulation by H-NS as a function of growth conditions depends on chromosomal position in Escherichia coli.

Brambilla E, Sclavi B - G3 (Bethesda) (2015)

(A) Global view of H-NS binding, AT content, and presence of tsEPODs in the E. coli chromosome. From the bottom to the top: The macrodomains, as defined by Boccard (Valens et al. 2004). Sites bound by H-NS in early exponential (HNS_EE), mid exponential (HNS_ME), transition to stationary (HNS_TS), and stationary phase (HNS_S) (Kahramanoglou et al. 2011). There is an increase in the number and the length of regions bound by H-NS when approaching stationary phase, especially in the terminus. tsEPODs mapped on the E. coli chromosome (Vora et al. 2009). The plot shows the number of genes overlapping with tsEPODs as determined from the NUST software, with multiple sliding windows histogram performed choosing a bin number equal to 32 (Scolari et al. 2012). The AT content is calculated with a sliding window of 50 kb with a shift of 10 kb. The two horizontal dashed lines correspond to 45 and 55% AT. The terminus shows greater AT-content. H-NS binding: sites bound by H-NS in the different growth phases (Kahramanoglou et al. 2011). (B−G) Genomic neighborhood of the chromosomal insertion positions of the reporter construct. From the bottom to the top of each plot: Genes on the lagging and on the leading strand. In gray, the two convergent genes between which the Phns-yfp construct was inserted. The site of insertion is shown by a red dot. Position of the sites bound by FIS in early exponential (FIS_EE) and in mid exponential (FIS_ME) phases (Kahramanoglou et al. 2011). There are more sites bound by FIS near the origin (LO and RO, plots on the top) than in the terminus (LT and RT, plots in the bottom). Position of the sites bound by H-NS in early exponential (HNS_EE), mid exponential (HNS_ME), transition to stationary (HNS_TS) and stationary (HNS_S) phases (Kahramanoglou et al. 2011). In the proximity of LT and RO there is an extended region of sites bound by H-NS. Presence of genes identified as transcriptionally silent (Vora et al. 2009). The AT content is calculated with a 4000-bp sliding window with a shift of 500 bases. The two horizontal dashed lines correspond to 45 and 55% AT. A peak in AT-content is visible near LT and RO. FIS, factor for inversion stimulation; H-NS, histone-like nucleoid-structuring protein; LM, left medium; LO, left origin; LT, left terminus; RM, right medium; RO, right origin; RT, right terminus; tsEPODs, transcriptionally silent extended protein occupancy domains.
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Related In: Results  -  Collection

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fig6: (A) Global view of H-NS binding, AT content, and presence of tsEPODs in the E. coli chromosome. From the bottom to the top: The macrodomains, as defined by Boccard (Valens et al. 2004). Sites bound by H-NS in early exponential (HNS_EE), mid exponential (HNS_ME), transition to stationary (HNS_TS), and stationary phase (HNS_S) (Kahramanoglou et al. 2011). There is an increase in the number and the length of regions bound by H-NS when approaching stationary phase, especially in the terminus. tsEPODs mapped on the E. coli chromosome (Vora et al. 2009). The plot shows the number of genes overlapping with tsEPODs as determined from the NUST software, with multiple sliding windows histogram performed choosing a bin number equal to 32 (Scolari et al. 2012). The AT content is calculated with a sliding window of 50 kb with a shift of 10 kb. The two horizontal dashed lines correspond to 45 and 55% AT. The terminus shows greater AT-content. H-NS binding: sites bound by H-NS in the different growth phases (Kahramanoglou et al. 2011). (B−G) Genomic neighborhood of the chromosomal insertion positions of the reporter construct. From the bottom to the top of each plot: Genes on the lagging and on the leading strand. In gray, the two convergent genes between which the Phns-yfp construct was inserted. The site of insertion is shown by a red dot. Position of the sites bound by FIS in early exponential (FIS_EE) and in mid exponential (FIS_ME) phases (Kahramanoglou et al. 2011). There are more sites bound by FIS near the origin (LO and RO, plots on the top) than in the terminus (LT and RT, plots in the bottom). Position of the sites bound by H-NS in early exponential (HNS_EE), mid exponential (HNS_ME), transition to stationary (HNS_TS) and stationary (HNS_S) phases (Kahramanoglou et al. 2011). In the proximity of LT and RO there is an extended region of sites bound by H-NS. Presence of genes identified as transcriptionally silent (Vora et al. 2009). The AT content is calculated with a 4000-bp sliding window with a shift of 500 bases. The two horizontal dashed lines correspond to 45 and 55% AT. A peak in AT-content is visible near LT and RO. FIS, factor for inversion stimulation; H-NS, histone-like nucleoid-structuring protein; LM, left medium; LO, left origin; LT, left terminus; RM, right medium; RO, right origin; RT, right terminus; tsEPODs, transcriptionally silent extended protein occupancy domains.
Mentions: The activity of the Phns promoter depends on the activation by the FIS protein in early exponential phase at fast growth (Falconi et al. 1996), Cold shock protein A (CspA) for induction upon cold shock (La Teana et al. 1991), and on the binding of the H-NS protein itself resulting in repression (Ueguchi et al. 1993; Falconi et al. 1993). Binding of the H-NS protein along the genome is not uniform and changes as a function of the growth phase (Kahramanoglou et al. 2011; Zarei et al. 2013). When the sites of insertion of the reporter construct are mapped on the H-NS binding patterns one can see that those sites that are less expressed (LT and RO) are found in regions with a greater probability of H-NS binding as measured by formaldehyde crosslinking (Figure 6 and Figure S4).

Bottom Line: Cellular adaptation to changing environmental conditions requires the coordinated regulation of expression of large sets of genes by global regulatory factors such as nucleoid associated proteins.Our results show that the activity of the Phns promoter depends on whether it is placed within the AT-rich regions of the genome that are known to be bound preferentially by H-NS.Genomic position can thus play a significant role in the adaptation of the cells to environmental changes, providing a fitness advantage that can explain the selection of a gene's position during evolution.

View Article: PubMed Central - PubMed

Affiliation: LBPA, UMR 8113 du CNRS, Ecole Normale Supérieure de Cachan, Cachan, France School of Engineering and Science, Jacobs University Bremen, Bremen, Germany.

Show MeSH
Related in: MedlinePlus