Coevolution of the Organization and Structure of Prokaryotic Genomes

Abstract

The cytoplasm of prokaryotes contains many molecular machines interacting directly with the chromosome. These vital interactions depend on the chromosome structure, as a molecule, and on the genome organization, as a unit of genetic information. Strong selection for the organization of the genetic elements implicated in these interactions drives replicon ploidy, gene distribution, operon conservation, and the formation of replication-associated traits. The genomes of prokaryotes are also very plastic with high rates of horizontal gene transfer and gene loss. The evolutionary conflicts between plasticity and organization lead to the formation of regions with high genetic diversity whose impact on chromosome structure is poorly understood. Prokaryotic genomes are remarkable documents of natural history because they carry the imprint of all of these selective and mutational forces. Their study allows a better understanding of molecular mechanisms, their impact on microbial evolution, and how they can be tinkered in synthetic biology.

Figure 1.

Traits associated with polyploidy in prokaryotes. The presence of multiple copies of replicons, and particularly chromosomes, has been proposed to confer several advantages. (A) It allows distributing gene expression through the entire cytoplasm in very large cells. It allows heterozygosity. In the presence of several replicons, the ratio between replicons allows gene expression regulation. (B) It allows repair by homologous recombination with other similar replicons. (C) Recombination between similar replicons also allows gene conversion and allelic exchange. Heterozygosity is indicated using distinct colors (red and black).

Figure 2.

Elements of genome organization. The cellular processes that interact with the chromosome shape its organization.

Figure 3.

The genetic organization of gene expression. (A) Schematic representation of the transcription factory model, in which multiple active RNA polymerases are concentrated at discrete sites in the nucleoid. (B) Bacterial genes are organized into operons, which group in superoperons. In addition to being physically close in the genome, genes in operons are cotranscribed, coregulated, and encode proteins involved in the same functional pathway or protein complex. Superoperons are not cotranscribed, but may share regulatory regions. (C) Schematic representation of three models aiming at explaining the formation and conservation of operons based on genetic linkage. (D) Transcription of genes in a single transcript is expected to diminish gene expression noise and ensure more precise stoichiometry. It also allows responding optimally to demand for a given pathway when the first genes to be transcribed are those starting the functional pathway. (E) Operons place several genes under the same regulatory region that is thus subject to more efficient selection.

Figure 4.

Balancing between genome organization and diversification. (A) Schematic representation of a model for the formation and evolution of integration hotspots. (B) Hotspots can be scattered in the chromosome. (C) Some chromosomes show very large regions in which most genetic diversification takes place. (D) Some chromosomes are very stable and most genetic diversification takes place in plasmids.