Impact of Chromosomal Architecture on the Function and Evolution of Bacterial Genomes

Abstract

The bacterial nucleoid is highly condensed and forms compartment-like structures within the cell. Much attention has been devoted to investigating the dynamic topology and organization of the nucleoid. In contrast, the specific nucleoid organization, and the relationship between nucleoid structure and function is often neglected with regard to importance for adaption to changing environments and horizontal gene acquisition. In this review, we focus on the structure-function relationship in the bacterial nucleoid. We provide an overview of the fundamental properties that shape the chromosome as a structured yet dynamic macromolecule. These fundamental properties are then considered in the context of the living cell, with focus on how the informational flow affects the nucleoid structure, which in turn impacts on the genetic output. Subsequently, the dynamic living nucleoid will be discussed in the context of evolution. We will address how the acquisition of foreign DNA impacts nucleoid structure, and conversely, how nucleoid structure constrains the successful and sustainable chromosomal integration of novel DNA. Finally, we will discuss current challenges and directions of research in understanding the role of chromosomal architecture in bacterial survival and adaptation.

Keywords: bacterial nucleoid structure; chromosomal architecture; gene expression; genome evolution; nucleoid associated proteins.

FIGURE 1

Intrinsic properties of DNA. (A) Basic coiled conformational states of DNA. In its relaxed state and under physiological conditions, DNA forms a double helix with 10.5 base pairs per turn. Introducing or removing turns causes the DNA to form local coiled elements either as twists in the linear dimension or by the formation of higher-order writhes (Corless and Gilbert, 2016). (B) Coiled conformational states of large DNA fragments. Two major higher-order supercoiled states of DNA, the stable plectonemic state and the less stable but more compact solenoidal state, emerge through extensive over- or under-winding of the DNA helix (Corless and Gilbert, 2016). (C) Rough sketch of the two basic molecular forms of DNA. At low hydration levels, DNA will take the A-form, the compact and wider helix form. At physiological conditions, DNA will adopt the more accessible B-form.

FIGURE 2

Extrinsic forces influencing the chromosome structure. (A) Intracellular levels of the major NAPs during growth phases (Not to scale) (Talukder and Ishihama, 1999, 2015). (B) Impact of different NAPs on the nucleoid superstructure (Badrinarayanan et al., 2015; Winardhi et al., 2015; Yamanaka et al., 2018). For detailed description of structural impact see Table 1.

FIGURE 3

Informational relay and the nucleoid structure. (A) Simplified representation of the Escherichia coli chromosome and its interactions with the DNA replication- and transcription machineries. (B) Sketch of how replication and transcription impact nucleoid structure through changes in supercoiling levels (Corless and Gilbert, 2016). (C) Depiction of how translation and transertion affects nucleoid structure by pulling the nucleoid toward the membrane (Bakshi et al., 2015). (D) Relative changes in the cellular level of individual sigma factors during distinct growth phases (Gruber and Gross, 2003). (E) Cellular levels of supercoiling and emergence of superhelical gradient across the nucleoid during distinct growth phases (Lal et al., 2016).

FIGURE 4

Cellular space occupied by the nucleoid (yellow) and the dispersion of RNA polymerase (blue) during shift from rapid growth to slow or stressed growth.

FIGURE 5

Global patterns of nucleoid organization. Positional gradients of rRNA operons and stress related genes on the genome of Escherichia coli (Yellow/Green triangles). Each half of the nucleoid is approximately of equal lengths, and the relative position of the DARS1/2 and datA elements to oriC is conserved among 59 highly different E. coli strains (orange boxes) (Frimodt-Møller et al., 2015, 2016; Riber et al., 2016). Furthermore, the number of genes transcribed against the replication fork is lower than the number of genes along the direction of the replication fork (blue arrows).

FIGURE 6

Transcriptional spill. Recruitment of RNAP to a gene will increase the likelihood that spatially close genes will interact with RNAP. Transcriptional spill is not apparent from the uncoiled linear organization of genes (bottom) but becomes apparent when considering spatial organization.