A novel plasmid-transcribed regulatory sRNA, QfsR, controls chromosomal polycistronic mRNAs in Agrobacterium tumefaciens

Plasmids are mobile DNAs that adjust host cell functions for their own amplification and dissemination. We identified QfsR, a small RNA, transcribed from the Ti plasmid in the phytopathogen Agrobacterium fabrum. QfsR is widely conserved throughout RepABC plasmids carried by Rhizobiaceae. Target prediction, expression analysis and site-direct mutagenesis experiments show that QfsR directly pairs within polycistronic mRNAs transcribed from chromosomes (involved in flagella apparatus and succinoglycan biosynthesis) and Ti plasmid (involved in conjugative transfer). QfsR leads to a coordinated expression of whole polycistronic mRNA molecules. Whereas a lack of QfsR induces motility and reduces succinoglycan production, its overproduction increases the quorum sensing signal accumulation and the Ti plasmid conjugative transfer. Based on these observations, we propose QfsR as a hub connecting regulatory networks of motility, succinoglycan biosynthesis and plasmid conjugative transfer. To our knowledge, QfsR is the first example of a plasmid-encoded sRNA that controls chromosomal polycistronic mRNAs. SignificancePlasmids represent an important cost for the hosting cell although some are beneficial under certain circumstances. Agrobacterium tumefaciens harboring Tumor inducing plasmid (pTi) are able to infect plants and to use specific resources produced by the infected cells. We characterized QfsR, a novel small RNA (sRNA) from pTi, that directly regulates plasmid polycistronic mRNA but also chromosomal ones. QfsR contributes to a fine-tuned regulation of bacterial motility, exopolysaccharide biosynthesis and conjugative dissemination of pTi. Our results report the first plasmid-encoded sRNA able to modify and coordinate cellular behaviour probably for the benefit of the plasmid dissemination and tight crosstalk between plasmid and chromosome. This could be widespread since QfsR homologs were predicted in other plasmids of Rhizobiaceae symbionts and pathogens.