sRNA-mediated RNA processing regulates bacterial cell division

Abstract

Tight control of cell division is essential for survival of most organisms. For prokaryotes, the regulatory mechanisms involved in the control of cell division are mostly unknown. We show that the small non-coding sRNA StsR has an important role in controlling cell division and growth in the alpha-proteobacterium Rhodobacter sphaeroides. StsR is strongly induced by stress conditions and in stationary phase by the alternative sigma factors RpoHI/HII, thereby providing a regulatory link between cell division and environmental cues. Compared to the wild type, a mutant lacking StsR enters stationary phase later and more rapidly resumes growth after stationary phase. A target of StsR is UpsM, the most abundant sRNA in the exponential phase. It is derived from partial transcriptional termination within the 5′ untranslated region of the mRNA of the division and cell wall (dcw) gene cluster. StsR binds to UpsM as well as to the 5′ UTR of the dcw mRNA and the sRNA-sRNA and sRNA-mRNA interactions lead to a conformational change that triggers cleavage by the ribonuclease RNase E, affecting the level of dcw mRNAs and limiting growth. These findings provide interesting new insights into the role of sRNA-mediated regulation of cell division during the adaptation to environmental changes.

A Complex Network of Sigma Factors and sRNA StsR Regulates Stress Responses in R. sphaeroides

“…The R. sphaeroides sRNA StsR shows very low abundance in the exponential phase but is highly abundant in the stationary phase [ 37 ]. To evaluate the effect of StsR on the transcriptome, we performed RNAseq analysis with wild type cells of R. sphaeroides and with a mutant (ΔStsR) lacking the stsR gene.…”

“…Seventeen protein-coding genes showed lower expression in the mutant, including znuB and znuC ( znuA missed the cut-off for p -value) for a zinc transporter and pufK , which is part of the photosynthesis gene cluster. Seventy two hours after inoculation to an OD 660nm of 0.2, Rhodobacter cells were in the late stationary phase and StsR was highly expressed [ 37 ]. Under these conditions 618 protein-coding genes showed higher expression in the mutant strain ( Supplementary Table S1 ).…”

“…RpoHI and RpoHII do not only regulate expression of protein-coding genes but also regulate expression of sRNAs with a role in the stress defense in R. sphaeroides [ 15 , 32 , 35 , 36 , 37 ] ( Figure 1 ). StsR (formerly RSs0827) was first described as an sRNA induced upon iron starvation [ 36 ], and was later found to be the most highly induced RNA in late stationary phase [ 1 , 34 ].…”

“…StsR (formerly RSs0827) was first described as an sRNA induced upon iron starvation [ 36 ], and was later found to be the most highly induced RNA in late stationary phase [ 1 , 34 ]. StsR is under control of RpoHI/RpoHII [ 37 ] and, therefore, induced by multiple stress factors such as heat and oxidative stress. This sRNA was named StsR (sRNA targeting sRNA) due to its binding to the sRNA UpsM.…”

“…[ 38 ]. UpsM is derived from the 5′ UTR of the dcw (cell division and cell wall) genes [ 38 ], and binding of StsR to UpsM and to the dcw 5′ UTR affects dcw gene expression (and consequently cell division) in trans and in cis [ 37 ]. Here, we demonstrate that StsR also affects several mRNAs for regulators of photosynthesis genes and photosynthesis gene expression, as well as expression of sRNAs with a role in photooxidative stress in the stationary phase; we identify the rpoE mRNA as one target of StsR.…”