Abstract
The evolution of gene order rearrangements within bacterial chromosomes is a fast process. Closely related species can have almost no conservation in long-range gene order. A prominent exception to this rule is a >40 kb long cluster of five core operons (secE-rpoBC-str-S10-spc-alpha) and three variable adjacent operons (cysS, tufB, and ecf) that together contain 57 genes of the transcriptional and translational machinery. Previous studies have indicated that at least part of this operon cluster might have been present in the last common ancestor of bacteria and archaea. Using 204 whole genome sequences, ∼2 Gy of evolution of the operon cluster were reconstructed back to the last common ancestors of the Gammaproteobacteria and of the Bacilli. A total of 163 independent evolutionary events were identified in which the operon cluster was altered. Further examination showed that the process of disconnecting two operons generally follows the same pattern. Initially, a small number of genes is inserted between the operons breaking the concatenation followed by a second event that fully disconnects the operons. While there is a general trend for loss of gene synteny over time, there are examples of increased alteration rates at specific branch points or within specific bacterial orders. This indicates the recurrence of relaxed selection on the gene order within bacterial chromosomes. The analysis of the alternation events indicates that segmental genome duplications and/or transposon-directed recombination play a crucial role in rearrangements of the operon cluster.
Highlights
It is generally accepted that all life on earth has evolved from a universal common ancestor which would entail that all life forms share a single ancestral gene order (Woese 2000; Koonin 2003, 2014; Forterre 2015; Booth et al 2016; Weiss et al 2018)
Operons in the ancestral operon clusters were defined according to the Escherichia coli nomenclature to be consistent with previous studies
The outgroup species in the phylogenetic analysis of the Bacilli suggest that the tufB operon was present in the last common ancestor of the Firmicutes which agrees with a previous study that suggests that the tuf duplication precedes the evolution of the Firmicutes (Lathe and Bork 2001)
Summary
It is generally accepted that all life on earth has evolved from a universal common ancestor which would entail that all life forms share a single ancestral gene order (Woese 2000; Koonin 2003, 2014; Forterre 2015; Booth et al 2016; Weiss et al 2018). The order of genes on the chromosome changed over time until selection, genetic drift and horizontal gene transfer (HGT) removed almost all traces of the last common gene order from modern chromosomes (Koonin et al 1996; Tatusov et al 1996). Despite this general trend there are a few genes that display a significant degree of synteny across the bacterial domain of life which suggests that this gene order was present in at least the last common ancestor of all bacteria.
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