The SNAP hypothesis: Chromosomal rearrangements could emerge from positive Selection during Niche Adaptation

Abstract

The relative linear order of most genes on bacterial chromosomes is not conserved over evolutionary timescales. One explanation is that selection is weak, allowing recombination to randomize gene order by genetic drift. However, most chromosomal rearrangements are deleterious to fitness. In contrast, we propose the hypothesis that rearrangements in gene order are more likely the result of selection during niche adaptation (SNAP). Partial chromosomal duplications occur very frequently by recombination between direct repeat sequences. Duplicated regions may contain tens to hundreds of genes and segregate quickly unless maintained by selection. Bacteria exposed to non-lethal selections (for example, a requirement to grow on a poor nutrient) can adapt by maintaining a duplication that includes a gene that improves relative fitness. Further improvements in fitness result from the loss or inactivation of non-selected genes within each copy of the duplication. When genes that are essential in single copy are lost from different copies of the duplication, segregation is prevented even if the original selection is lifted. Functional gene loss continues until a new genetic equilibrium is reached. The outcome is a rearranged gene order. Mathematical modelling shows that this process of positive selection to adapt to a new niche can rapidly drive rearrangements in gene order to fixation. Signature features (duplication formation and divergence) of the SNAP model were identified in natural isolates from multiple species showing that the initial two steps in the SNAP process can occur with a remarkably high frequency. Further bioinformatic and experimental analyses are required to test if and to which extend the SNAP process acts on bacterial genomes. Author summaryAll life on earth has evolved from a universal common ancestor with a specific order of genes on the chromosome. This order is not maintained in modern species and the standard hypothesis is that changes reflect a lack of strong selection on gene order. Here, we propose an alternative hypothesis, SNAP. The occupation of a novel environment by bacteria is generally a trade-off situation. For example, while the bacteria may not be adapted PLOS Genetics | https://doi.org/10.1371/journal.pgen.

Reconstructing the Evolutionary History of a Highly Conserved Operon Cluster inGammaproteobacteriaandBacilli

“…Subsequently, the asymmetrical loss of duplicate genes can lead to alterations in the gene order on the chromosome ( fig. 7 ) ( Brandis and Hughes 2020 ). Segmental duplications are probably the most common type of mutations in the bacterial genome as they appear at very high frequencies even in the absence of selection ( Anderson and Roth 1977 ; Haack and Roth 1995 ; Reams et al 2010 ), are often found during laboratory selection conditions ( Riehle et al 2001 ; Knöppel et al 2016 ), and play a role in shaping genome diversification and the evolution of new genes ( Bergthorsson et al 2007 ; Näsvall et al 2012 ; Zhou et al 2012 ).…”

“…The subsequent loss of duplicate genes/operons is a slow process enabling the bacteria to adapt to potential negative consequences caused by the novel gene order. Thus, the SNAP model could explain the observed operon cluster alterations by combining high-frequency events and overcoming counter-selective barriers ( Brandis and Hughes 2020 ). This model could also explain the duplicate section of the operon cluster ( rpmJ - rpsM - rpsK - rpsD - rpoA - rplQ ) found in P .…”

High Rates of Genome Rearrangements and Pathogenicity of Shigella spp.

“…These events are largely detrimental for free-living bacteria and are expected to be selected against (Darling et al, 2008). On the other hand, in a new environment, non-homologous recombination and the associated functional changes may provide a base for adaptation (Yan et al, 2018;Brandis and Hughes, 2020). For instance, Burkholderia mallei, a young obligate intracellular pathogen, has lost numerous clusters of genes through IS-mediated elimination as demonstrated by the comparison of its genome to strains of the ancestral species, Burkholderia pseudomallei (Losada et al, 2010;Bochkareva et al, 2018a).…”

High rates of genome rearrangements and pathogenicity ofShigellaspp

“…These events are largely detrimental for free-living bacteria and are expected to be selected against (18). On the other hand, in a new environment, non-homologous recombination and the associated functional changes may provide a base for adaptation (46, 47). For instance, Burkholderia mallei , a young obligate intracellular pathogen, has lost numerous clusters of genes through IS-mediated elimination as demonstrated by the comparison of its genome to strains of the ancestral species, Burkholderia pseudomallei (48, 49).…”