Xenogeneic Silencing and Bacterial Genome Evolution: Mechanisms for DNA Recognition Imply Multifaceted Roles of Xenogeneic Silencers

Abstract

Horizontal gene transfer (HGT) is a major driving force for bacterial evolution. To avoid the deleterious effects due to the unregulated expression of newly-acquired foreign genes, bacteria have evolved specific proteins named xenogeneic silencers to recognize foreign DNA sequences and suppress their transcription. As there is considerable diversity in genomic base compositions among bacteria, how xenogeneic silencers distinguish self- from non-self DNA in different bacteria remains poorly understood. This review summarizes the progress in studying the DNA binding preferences and the underlying molecular mechanisms of known xenogeneic silencer families, represented by H-NS of Escherichia coli, Lsr2 of Mycobacterium, MvaT of Pseudomonas, and Rok of Bacillus. Comparative analyses of the published data indicate that the differences in DNA recognition mechanisms enable these xenogeneic silencers to have clear characteristics in DNA sequence preferences, which are further correlated with different host genomic features. These correlations provide insights into the mechanisms of how these xenogeneic silencers selectively target foreign DNA in different genomic backgrounds. Furthermore, it is revealed that the genomic AT contents of bacterial species with the same xenogeneic silencer family proteins are distributed in a limited range, and are generally lower than those species without any known xenogeneic silencers in the same phylum/class/genus, indicating that xenogeneic silencers have multifaceted roles on bacterial genome evolution. In addition to regulating horizontal gene transfer, xenogeneic silencers also act as a selective force against the GC to AT mutational bias found in bacterial genomes and help the host genomic AT contents maintained at relatively low levels.

Xenogeneic silencing strategies in bacteria are dictated by RNA polymerase promiscuity

“…Like H-NS analogues in other organisms, the B. subtilis Rok protein recognises horizontally acquired AT-rich DNA 33 . In particular, Rok preferentially binds DNA sequences with TpA steps, rather than continuous A or T tracts 29 , 33 . Such sequences are ideal templates for transcription initiation events 14 , 15 , 34 .…”

HI-NESS: a family of genetically encoded DNA labels based on a bacterial nucleoid-associated protein

“…This observation also implies that HI-NESS is not a suitable DNA stain for use in E. coli . HI-NESS is also unsuitable in bacteria that express H-NS-like proteins that tend to show a preference for AT-rich sequences ( 78 , 79 ). The distribution of HI-NESS and that of mEos3.2 without the DNA binding moiety in Mycobacterium marinum , an organism that expresses the H-NS-like nucleoid-associated protein Lsr2, was indistinguishable ( Supplementary Figure S1 ).…”

Phylogenetic Distribution of WhiB- and Lsr2-Type Regulators in Actinobacteriophage Genomes

“…Lsr2-like proteins have already been described as xenogeneic silencers that repress the expression of ‘foreign’, AT-rich DNA elements in host genomes ( 16 , 17 , 20 , 37 ). Because foreign DNA in the form of viruses is one of the most primordial threats in the evolution of life, the role of Lsr2-like proteins in the control of the phage gene expression is probably ancient.…”