Absence of Ribosome Modulation Factor Alters Growth and Competitive Fitness of Escherichia coli

Hans, Sebastian; Finkel, Steven E.

doi:10.1128/spectrum.02239-21

Cited by 7 publications

(6 citation statements)

References 43 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The next important step will be to understand how bacterial cells could benefit from having Balon. Because both Rmf and RaiA protect ribosomes from nucleolytic degradation during starvation and stress [11][12][13] , it is possible that Balon functions in an analogous manner, protecting the ribosomal A site that remains vulnerable even in the presence of Rmf and RaiA (Fig. S9).…”

Section: Balon As a Factor Involved In Ribosomal Dormancymentioning

confidence: 99%

“…Here we find that Balon binds and occupies the A site of at least 66 % of ribosomes in P. urativorans cells in response to ice treatment, thus making Balon functionally analogous to such factors as bacterial Rmf and RaiA and eukaryotic Stm1 23 , Serpbp1 19 , Irfd2 24,25 , Lso2 [26][27][28] , and Mdf1 29,30 . RaiA and Rmf have been shown to enhance bacterial survival by protecting ribosomes from nucleolytic degradation during starvation or stress [16][17][18] , and it is likely that Balon functions in a similar but non-redundant manner. Our structural studies suggest that Balon protects features of the A site that remain vulnerable even in the presence of RaiA and Rmf (Fig.…”

Section: Balon Is a Novel Factor Of Bacterial Ribosome Dormancymentioning

confidence: 99%

“…Nonetheless, all dormancy factors share one property: their ability to protect the most critically important functional sites in the ribosome, such as the mRNA channel and tRNA-binding sites 9 . Furthermore, some dormancy factors have nonoverlapping binding sites, making it possible for the ribosome to simultaneously bind several dormancy factors [11][12][13]26 . However, the lack of universal conservation of ribosome dormancy factors, along with a small number of suitable organisms to study ribosome dormancy, leaves it unclear to what extent findings made in common model organisms-mainly E. coli -can be considered generally representative.…”

Section: Introductionmentioning

confidence: 99%

“…Although the reversible arrest of protein synthesis was initially viewed as a passive process in which ribosomes remain idle and free from ligands, it has become clear in recent years that, during starvation and stress, ribosomes associate with a specialized group of cellular proteins known as hibernation factors or dormancy factors 9,10 . These factors bind to ribosomes, shielding their vulnerable active centres from degradation by cellular nucleases [11][12][13] . Due to this critical protective role, the depletion of dormancy factors causes the accumulation of damaged ribosomes and drastically impairs the ability of cells to recover their growth after starvation, stress, or drug treatment [14][15][16][17] .…”

Section: Introductionmentioning

confidence: 99%

“…Initial studies of ribosome hibernation factors suggested they may arrest protein synthesis due to their occupation of ribosomal binding sites for mRNA and tRNAs 14,15 . However, recent biochemical and genetic studies have revealed that dormancy factors also protect ribosomes from degradation by shielding their vulnerable active centres from cleavage by cellular nucleases [16][17][18] . Therefore, when ribosome hibernation factors are depleted through genetic knockouts, cells do not lose their ability to arrest protein synthesis in response to stress; rather, these cells rapidly accumulate defective ribosomes, causing a slower or incomplete recovery from stress.…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

A bacterial ribosome hibernation factor with evolutionary connections to eukaryotic protein synthesis

Helena-Bueno

Ekemezie

Brown

et al. 2022

Preprint

View full text Add to dashboard Cite

During starvation and stress, virtually all organisms arrest their protein synthesis and convert their ribosomes into a state of dormancy in which a special class of proteins, known as hibernation factors, protect the ribosome from damage. In bacteria, two major families of hibernation factors have been characterized, but the low conservation of these proteins and the huge diversity of species, habitats and environmental stressors has made the discovery of new dormancy factors challenging. In this study, we identify a new bacterial protein involved in ribosome dormancy. We first characterize dormant ribosomes following cold shock in the psychrophilic bacterium Psychrobacter urativorans using proteomics and cryo-EM. We show that during cold shock, ribosomes in this organism associate with a previously uncharacterized protein that occupies ribosomal active centres and multiple drug-binding sites. Our structure reveals that this new factor, which we term Balon, bears no resemblance to known bacterial hibernation factors. Instead, it belongs to a family of bacterial homologs of the eukaryotic translation factor aeRF1. We identify unique motifs present only in Balon but not its archaeal or eukaryotic counterparts that allow it to engage with the peptidyl transferase center and decoding center of dormant bacterial ribosomes. We then show that, across the bacterial kingdom, Balon-encoding genes are found in nearly 20% of known species and are located in operons involved in different types of stress responses, including osmotic and thermal shock, hypoxia, acid, tRNA damage and antibiotic stress. Taken together, our work shows that bacterial cells possess a functional homolog of eukaryotic translation termination factor, which is likely repurposed into a stress-response protein. This finding illuminates a long-sought evolutionary connection between the bacterial and eukaryotic protein synthesis machinery.

show abstract

Section: Balon As a Factor Involved In Ribosomal Dormancymentioning

confidence: 99%