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EcoSal Plus

Domain 2: Cell Architecture and Growth

Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: Andrew Travers1,2, and Georgi Muskhelishvili3
  • Editors: James M. Slauch4, Olivier Espeli5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: MRC Laboratory of Molecular Biology, Cambridge Biomedical Campus, Cambridge, UK; 2: Department of Biochemistry, University of Cambridge, Cambridge, UK; 3: Agricultural University of Georgia, 0159 Tbilisi, Georgia; 4: The School of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL; 5: Center for Interdisciplinary Research in Biology (CIRB), College de France, CNRS, INSERM, Paris, France
  • Received 14 April 2019 Accepted 03 December 2019 Published 13 February 2020
  • Address correspondence to Georgi Muskhelishvili, [email protected]
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  • Abstract:

    In this article, we summarize our current understanding of the bacterial genetic regulation brought about by decades of studies using the model. It became increasingly evident that the cellular genetic regulation system is organizationally closed, and a major challenge is to describe its circular operation in quantitative terms. We argue that integration of the DNA analog information (i.e., the probability distribution of the thermodynamic stability of base steps) and digital information (i.e., the probability distribution of unique triplets) in the genome provides a key to understanding the organizational logic of genetic control. During bacterial growth and adaptation, this integration is mediated by changes of DNA supercoiling contingent on environmentally induced shifts in intracellular ionic strength and energy charge. More specifically, coupling of dynamic alterations of the local intrinsic helical repeat in the structurally heterogeneous DNA polymer with structural-compositional changes of RNA polymerase holoenzyme emerges as a fundamental organizational principle of the genetic regulation system. We present a model of genetic regulation integrating the genomic pattern of DNA thermodynamic stability with the gene order and function along the chromosomal OriC-Ter axis, which acts as a principal coordinate system organizing the regulatory interactions in the genome.

  • Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019

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/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0016-2019
2020-02-13
2020-07-16

Abstract:

In this article, we summarize our current understanding of the bacterial genetic regulation brought about by decades of studies using the model. It became increasingly evident that the cellular genetic regulation system is organizationally closed, and a major challenge is to describe its circular operation in quantitative terms. We argue that integration of the DNA analog information (i.e., the probability distribution of the thermodynamic stability of base steps) and digital information (i.e., the probability distribution of unique triplets) in the genome provides a key to understanding the organizational logic of genetic control. During bacterial growth and adaptation, this integration is mediated by changes of DNA supercoiling contingent on environmentally induced shifts in intracellular ionic strength and energy charge. More specifically, coupling of dynamic alterations of the local intrinsic helical repeat in the structurally heterogeneous DNA polymer with structural-compositional changes of RNA polymerase holoenzyme emerges as a fundamental organizational principle of the genetic regulation system. We present a model of genetic regulation integrating the genomic pattern of DNA thermodynamic stability with the gene order and function along the chromosomal OriC-Ter axis, which acts as a principal coordinate system organizing the regulatory interactions in the genome.

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Figures

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Figure 1

(A) Systems-theoretical view of operationally closed circuit indicated by an arrow closing on to itself. (B) Organization of unity by coupling two logically different (analog and digital) types of information standing in relationship of reciprocal determination. Note that while the system exchanges energy and matter with the environment, its operation is entirely determined by its internal structure ( 2 ).

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Figure 2

(A) Distribution of anabolic genes. (B) Distribution of catabolic genes. The chromosome is linearized at the origin of replication OriC, whereas the terminus (Ter) is in the middle. The number of relevant genes relative to the total number of genes within the window is counted and normalized to [0;1]. Data from reference 17 .

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Figure 3

First bar: Genes on the clockwise (right) replichore are above the bar, and genes on the counterclockwise (left) replichore are below the bar. Selected genes involved in the control of DNA topology. , a component of DNA gyrase responsible for increasing negative superhelicity, maps close to OriC, whereas the gyrase inhibitor, susceptibility to B17 microcin locus C (sbmC), and and , both responsible for relaxing DNA, map either close to or within the Ter macrodomain. The DNA gyrase inhibitor (), encoding an inhibitor of GyrB, maps close to the center. Chromosomal partition genes C and E ( and ) encode the subunits of topoisomerase IV, responsible for decatenation of newly replicated DNA in the terminal region ( 239 ) and relaxation of negative supercoils ( 240 ). Second bar: Selected genes encoding NAPs. The NAP-encoding gene closest to OriC is , encoding histone-like protein from strain U93 (HUα). Its early expression relative to , encoding HUβ ( 241 ), could buffer high negative superhelicity generated by DNA gyrase. A mutation in both increases the growth rate and antagonizes the histone-like nucleoid-structuring protein (H-NS) regulation of certain transcription units ( 242 ). is activated by ppGpp ( 243 ) on transition to stationary phase. Third bar: Selected genes involved in modulating RNAP activity, including σ factor-utilization regulators, secondary channel-binding proteins, termination/elongation factors, and RNAP subunits. σ factor-utilization regulators (light green): the ω subunit of RNA polymerase (), mapping close to the origin, encodes the ω subunit of RNAP, which confers a preference for utilization of σ ( 167 ). Regulator of sigma D () encodes an anti-σ ( 244 ), whereas confers a strong preference for σ utilization ( 245 ). Note that both and map closer to OriC than do the respective σ factors whose activity they affect. The encoded regulatory pattern thus reflects a shift from predominantly σ use close to OriC to σ availability in the central region of the chromosome. Secondary channel-binding proteins (pink): the transcription elongation factors ( and ) both map in the region containing many genes expressed during rapid growth. DksA inhibits ribosomal protein promoters and initiation ( 170 , 246 ) and is more distant from OriC than is . , it would act to reduce the rate of initiation and hence antagonize transcription foci formation. Termination/elongation factors (red): The termination factor Rho is encoded by a gene located very close to OriC. This location may compensate for the antagonistic effect of high negative superhelicity on transcription termination, which involves the rewinding of DNA. RNAP subunits: The map positions relative to OriC of and , encoding σ and σ, respectively, correspond to their relative order of temporal expression ( 33 ). Data from reference 18 .

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Figure 4

The latter is divided into four phases: early (also known as lag), mid (also known as log or exponential), late (also known as postexponential or transition), and stationary, characterized by different expression patterns. (A) The growth time after the shift up is indicated in minutes on the abscissa, and the relative frequencies of expressed genes are indicated on the ordinate. The RNA expression patterns are obtained from reference 33 . The different curves were normalized to [0;1] to compare them in one plot. (B to D) The growth phase-dependent expression of various transcription machinery components (B) and NAPs (C and D). The latter patterns should be compared with the levels of expressed protein ( 247 ).

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Figure 5

Abscissa, time after inoculation; ordinate, relative frequency of different orientations of genes. The plot shows the temporal impact of different gene orientations on gene expression. The different curves were normalized to [0;1] to compare them in one plot. The envelopes of the curves indicate the standard deviation at 10% random remapping of the expression patterns to genes. The minimum and maximum values are indicated in brackets in the legend. The expression values in brackets are normalized to the expression of all genes. Optical density and partial oxygen pressure are indicated by the dashed brown and blue lines, respectively.

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Figure 6

The time after the nutritional shift up is indicated in minutes on the abscissa, and the relative frequencies of expressed genes are indicated on the ordinate. The patterns of genes requiring high negative superhelical density (blue curve) and DNA relaxation (red curve), as well as the distance of the expressed genes to the OriC (yellow) and their average negative melting energy (black) are shown. The different curves were normalized to [0;1] to compare them in one plot. The envelopes of the curves indicate the standard deviation at 10% random remapping of the expression patterns to genes. The minimum and maximum values are indicated in brackets in the legend. The expression values in brackets are normalized to the expression of all genes. Optical density and partial oxygen pressure are indicated by the dashed green and blue lines, respectively.

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Figure 7

The chromosomal macrodomains are color-coded and indicated on the circular genome (outer ring). The blue star indicates the junction of the left and left nonstructured domains. The genomic wheels (inner ring) below the macrodomain rings show the distributions of the average negative melting energy (–ve ME) with blue for high and red for low (colormap). (A) GO-tree connections reflecting functional relatedness (MAGOG). (B) TRN. (C) Couplon network (Couplon). (D) HETNet connections. (E and F) Communication patterns of the cells harvested during fast exponential growth (E) and on transition to the stationary phase (F). The genomic wheels (inner ring) below the macrodomain rings (outer ring) represent the distribution of gene expression densities in the circular chromosome and show the significantly increased (red), decreased (blue), or constant (green) gene expression densities (GED, indicated by colormap) according to the depicted stages. Significantly increased and decreased HETNet connectivity (Conct) patterns between the chromosomal regions are indicated, respectively, by red and blue connecting lines; black lines indicate static communications absent in the expression profile. The positions of OriC and Ter, as well as the chromosomal macrodomains, are indicated. Note the repression of the chromosomal OriC end and activation of the Ter end on transition of cells to stationary phase. Data from reference 18 .

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Figure 8

(A) Stress response of d3. The domain is represented in the form of squares composed of four rectangles corresponding to four different growth media numbered 1 to 4. The squares are arranged in two rows corresponding to different stress conditions (acidic for the upper and oxidative for the lower) applied during exponential growth. The seven columns corresponding to the analyzed parameters indicated above include the gene expression density (dens), average melting energy (melt), and response to high negative superhelicity (hyp), to DNA relaxation (rel), and to the NAPs. The upward and downward arrows indicate the genes, respectively, activated or repressed by the indicated NAPs. The changes of color in each row of the squares indicate the difference (red, increase; blue, decrease; green, no change) from the rows of the previous square (oxidative stress is compared to acidic, whereas acidic stress is compared to untreated cells). (B) Response of the chromosomal d7 to the osmotic (upper row) and oxidative (lower row) stresses applied in the stationary phase (oxidative stress is compared to osmotic, whereas osmotic stress is compared to untreated cells). The representation is as in panel A. Data from reference 204 .

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Figure 9

Summary of the correlation between the DNA helical repeat and NAP binding related to the geometry of the interwindings and apical loops of DNA plectonemes. In the Dps-DNA complex, the helical repeat of the bound DNA is undetermined. In an analogous situation in , the DNA bound by the spore-specific acid-soluble proteins associated with spore DNA has a helical repeat of ∼11.5 bp ( 248 ), while some of the highly condensed DNA encapsidated in the phage T5 and certain archaeal viruses is crystalline A-form ( 231 , 249 ).

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019
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Tables

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Table 1

Correlation of changes in nucleoid area, expression of genes encoding NAPs, and polymerase components during the growth cycle

Citation: Travers A, Muskhelishvili G. 2020. Chromosomal Organization and Regulation of Genetic Function in Integrates the DNA Analog and Digital Information, EcoSal Plus 2020; doi:10.1128/ecosalplus.ESP-0016-2019

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