Evolution of Genome Architecture in Archaea: Spontaneous Generation of a New Chromosome in Haloferax volcanii

Abstract

The common ancestry of archaea and eukaryotes is evident in their genome architecture. All eukaryotic and several archaeal genomes consist of multiple chromosomes, each replicated from multiple origins. Three scenarios have been proposed for the evolution of this genome architecture: 1) mutational diversification of a multi-copy chromosome; 2) capture of a new chromosome by horizontal transfer; 3) acquisition of new origins and splitting into two replication-competent chromosomes. We report an example of the third scenario: the multi-origin chromosome of the archaeon Haloferax volcanii has split into two elements via homologous recombination. The newly generated elements are bona fide chromosomes, because each bears “chromosomal” replication origins, rRNA loci, and essential genes. The new chromosomes were stable during routine growth but additional genetic manipulation, which involves selective bottlenecks, provoked further rearrangements. To the best of our knowledge, rearrangement of a naturally evolved prokaryotic genome to generate two new chromosomes has not been described previously.

Whole‐genome comparison between the type strain of Halobacterium salinarum (DSM 3754T) and the laboratory strains R1 and NRC‐1

“…For example, the large plasmid pHV4 of Hfx. volcanii can stably insert into the main chromosome (Ausiannikava et al, ; Hawkins, Malla, Blythe, Nieduszynski, & Allers, ) taking with it an origin of replication. Our analyses can, however, not distinguish between different genome variants in distinct cells or variants within a single cell, although the latter is less likely to be encountered.…”

Probabilistic model based on circular statistics for quantifying coverage depth dynamics originating from DNA replication

“…We used the von Mises distribution for mixing because it has an intermediate degree of density around the mode and an open range of concentration parameters; i.e., κ > 0. Both genomic and short-read sequences were obtained according to the procedures described previously (Ausiannikava et al, 2018;Payne et al, 2018). The coverage depth was calculated according to the above-mentioned procedure.…”

“…To demonstrate the extendibility of our method, we modeled the coverage depth behavior of multiple replication origins, using a mixture of circular distributions. To validate our model, we applied it to WGS data of Sulfolobus solfataricus and Haloferax volcanii, which contain three replication origins (Ausiannikava et al, 2018;Payne et al, 2018). Based on the AIC and WAIC, we determined the number of components in both datasets to be three because this number yielded the best score on average (Table S10).…”

Peer Review #2 of "Probabilistic model based on circular statistics for quantifying coverage depth dynamics originating from DNA replication (v0.1)"

“…Finally, the highest log-likelihood in 30 independent trials was used as a representative estimate. short-read sequences were obtained according to the procedures described previously (Ausiannikava et al, 2018;Payne et al, 2018). The coverage depth was calculated according to the above-mentioned procedure.…”

“…To demonstrate the extendibility of our method, we modeled the coverage depth behavior of multiple replication origins, using a mixture of circular distributions. To validate our model, we applied it to WGS data of Sulfolobus solfataricus and Haloferax volcanii, which contain three replication origins (Ausiannikava et al, 2018;Payne et al, 2018). Based on the AIC and WAIC, we determined the number of components in both datasets to be three because this number yielded the best score on average (Supplementary Table 10).…”