A new beginning with new ends: linearisation of circular chromosomes during bacterial evolution

Abstract

Bacterial circular chromosomes have sporadically become linearised during prokaryote evolution. Unrelated bacteria, including the spirochete Borrelia burgdorferi and the actinomycete Streptomyces, have linear chromosomes. Linear chromosomes may have been formed through integration of linear plasmids. Linear chromosomes use linear plasmid strategies to resolve the 'end-of-replication problem', but they have generally retained from their circular ancestors a central origin of replication. Streptomyces linear chromosomes are very unstable and at high frequency undergo amplifications and large deletions, often removing the telomeres. At least in Streptomyces, chromosome linearity is reversible: circular chromosomes arise spontaneously as products of genetic instability or can be generated artificially by targeted recombination. Streptomyces circularised chromosomes are very unstable as well, indicating that genetic instability is not confined to the linearised chromosomes. Bacterial linear chromosomes may contain telomere-linked regions of enhanced genomic plasticity, which undergo more frequent genetic exchanges and rearrangements and allow differential evolution of genes, depending on their chromosomal location.

Telomere maintenance, function and evolution: the yeast paradigm

“…Thus, the condition of a strict structural conservation is unnecessary for telomere evolution. The ability to easily resolve the Bendreplication problem^appears to be a universal property of life, since bacterial circular chromosomes have sporadically become linearized during prokaryote evolution (Volff & Altenbuchner 2000) and sequence patterns at the ends of the linear genome of an archaeal virus is reminiscent of eukaryotic telomeric ends (Prangishvili & Garrett 2004). Regarding yeast telomere evolution, we propose that RNA template mutations conforming to a certain level of TG-richness and protein binding specificity have been frequently fixed in yeast populations.…”

Complete genome sequencing of Agrobacterium sp. H13-3, the former Rhizobium lupini H13-3, reveals a tripartite genome consisting of a circular and a linear chromosome and an accessory plasmid but lacking a tumor-inducing Ti-plasmid

“…3b). It has been observed that the ends of linear chromosomes represent regions of enhanced genomic plasticity (Chen et al, 2002;Volff and Altenbuchner, 2000). For example, linear chromosomes can undergo interchromosomal recombination between short homologous segments which might lead to the translocation of chromosomal blocks (Chen et al, 2002;Volff and Altenbuchner, 2000).…”

“…Thus, it appears that the ends of linear Agrobacterium chromosomes seem to be less well conserved compared to central parts of these replicons. It has been discussed that enhanced plasticity at the ends of linear chromosomes might facilitate genome adaptation and rearrangements (Volff and Altenbuchner, 2000). A prerequisite for the development of linear chromosomes is the existence of a telomerase gene (telA) in the genome.…”

Description of Streptomyces neopeptinius sp. nov., an actinobacterium with broad spectrum antifungal activities

“…Streptomycetes are mostly known as the representative antibioticproducing prokaryotic group, while many other interesting features such as morphological differentiation including mycelial growth and formation of arthrospores, and genetic properties including linear chromosomes and genetic instability, have also been the subjects of scientific interests (Locci, 1987;Volff and Altenbuchner, 2000;Chen et al, 2002). The production of antifungal substances is a common phenomenon among streptomycetes, as a number of such substances have been discovered to date (Table 1).…”