Horizontally Acquired Homologs of Xenogeneic Silencers: Modulators of Gene Expression Encoded by Plasmids, Phages and Genomic Islands

Abstract

Acquisition of mobile elements by horizontal gene transfer can play a major role in bacterial adaptation and genome evolution by providing traits that contribute to bacterial fitness. However, gaining foreign DNA can also impose significant fitness costs to the host bacteria and can even produce detrimental effects. The efficiency of horizontal acquisition of DNA is thought to be improved by the activity of xenogeneic silencers. These molecules are a functionally related group of proteins that possess affinity for the acquired DNA. Binding of xenogeneic silencers suppresses the otherwise uncontrolled expression of genes from the newly acquired nucleic acid, facilitating their integration to the bacterial regulatory networks. Even when the genes encoding for xenogeneic silencers are part of the core genome, homologs encoded by horizontally acquired elements have also been identified and studied. In this article, we discuss the current knowledge about horizontally acquired xenogeneic silencer homologs, focusing on those encoded by genomic islands, highlighting their distribution and the major traits that allow these proteins to become part of the host regulatory networks.

Ancestral zinc-finger bearing protein MucR in alpha-proteobacteria: A novel xenogeneic silencer?

“…Consequently, co-transfer of MucR and AT-rich target genes can be one of the important mechanisms balancing adaptation and regulatory integration. This hypothesis is in line with the view that AT-rich foreign genes providing adaptive benefits to recipients under ever-changing circumstances should however be tightly controlled to avoid unnecessary metabolic burden and toxicity [3] , [65] , [66] , [67] . When we look at the complete genome of Methylobacterium sp.…”

“…Certain homologs of H-NS, MvaT, Rok and Lsr2 were also identified in horizontally transferable genomic islands [68] , plasmids [69] , [70] , or bacteriophages [71] , [72] . Their known and potential roles in modulating expression of co-transferred genes and host genes [66] highlight that XSs are important players in managing the evolution of pangenome, which is essential for prokaryotes to explore the unlimited niches on the earth.…”

Redefining the H-NS protein family: a diversity of specialized core and accessory forms exhibit hierarchical transcriptional network integration

“…Here, we present a phylogenetic reconstruction of the H-NS protein family in Enterobacterales, revealing an unexpected diversity of chromosomal and plasmid-borne homologs. In the scientific literature, H-NS homologs are usually referred to as ‘H-NS paralogs’ due to a presumed evolutionary origin of hns duplication and diversification ( 20 , 40 , 85 ). However, our phylogenetic reconstruction of H-NS family evolution in the Enterobacterales demonstrates that StpA, Sfh and Hfp are homologs but are not paralogs.…”

“…In contrast, the Hfp clade contains extensive diversity, and the phylogeny in Supplementary Figure S3B illustrates how the hfp gene has moved horizontally within and between the bacterial families Enterobacteriaceae and Pectobacteriaceae. EARL islands are excisable and mobilizable ( 20 ), explaining the horizontal transmission of hfp genes. Future research will examine the mobility of hfp when it is not associated with EARL islands, as in Brenneria and Dickeya , in some cases in Pectobacterium , and at the serU-tRNA locus in E. coli .…”

“…Typhimurium, Sfh can act as a ‘stealth factor’ that protects host cells from uncontrolled expression of chromosomal and plasmid-encoded genes caused by H-NS binding to newly arrived plasmid genes ( 39 ). Thus, stealth function is explained as an extension of the xenogeneic silencing exhibited by H-NS ( 20 ).…”