Inactivation of Ribosomal Protein Genes in Bacillus subtilis Reveals Importance of Each Ribosomal Protein for Cell Proliferation and Cell Differentiation

Akanuma, Genki; Nanamiya, Hideaki; Natori, Yousuke; Yano, Koichi; Suzuki, Shota; Omata, Shuya; Ishizuka, Morio; Sekine, Yoshiaki; Kawamura, Fujio

doi:10.1128/jb.01544-12

Cited by 92 publications

(110 citation statements)

References 64 publications

(92 reference statements)

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“…It was recently shown that the deletion of the rpsU gene (encoding the S21 ribosomal protein) led to the formation of a small circle of a swarm colony (Akanuma et al, 2012). To assess the effect of rrn copy number on motility, we measured the swarm circles for the ten strains on LB agar plates containing 0.4 % Bacto agar.…”

Section: Motility Of Cells Carrying One To Ten Copies Of the Rrn Operonmentioning

confidence: 99%

Multiple rRNA operons are essential for efficient cell growth and sporulation as well as outgrowth in Bacillus subtilis

et al. 2013

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The number of copies of rRNA (rrn) operons in a bacterial genome differs greatly among bacterial species. Here we examined the phenotypic effects of variations in the number of copies of rRNA genes in the genome of Bacillus subtilis by analysis of eight mutant strains constructed to carry from two to nine copies of the rrn operon. We found that a decrease in the number of copies from ten to one increased the doubling time, and decreased the sporulation frequency and motility. The maximum levels for transformation activity were similar among the strains, although the competence development was significantly delayed in the strain with a single rrn operon. Normal sporulation only occurred if more than four copies of the rrn operon were present, although ten copies were needed for vegetative growth after germination of the spores. This behaviour was seen even though the intracellular level of ribosomes was similar among strains with four to ten copies of the rrn operon. Furthermore, ten copies of the rrn operon were needed for the highest swarming activity. We also constructed 21 strains that carried all possible combinations of two copies of the rrn operons, and found that these showed a range of growth rates and sporulation frequencies that all fell between those recorded for strains with one or three copies of the rrn operon. The results suggested that the copy number of the rrn operon has a major influence on cellular processes such as growth rate and sporulation frequency.

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Section: Motility Of Cells Carrying One To Ten Copies Of the Rrn Operonmentioning

confidence: 99%

Multiple rRNA operons are essential for efficient cell growth and sporulation as well as outgrowth in Bacillus subtilis

et al. 2013

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“…In bacteria, the severity of the growth phenotypes of ribosomal mutants can depend strongly on the growth conditions, especially the growth temperature (Akanuma et al, 2012). Therefore, we tested the Drps15/Drpl33 double knockout for survival under different temperatures.…”

Section: Rescue Of the Synthetic Lethality Of The Drps15/drpl33 Doublmentioning

confidence: 99%

Synthetic Lethality in the Tobacco Plastid Ribosome and Its Rescue at Elevated Growth Temperatures

et al. 2014

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ORCID ID: 0000-0001-7502-6940 (R.B.)Consistent with their origin from cyanobacteria, plastids (chloroplasts) perform protein biosynthesis on bacterial-type 70S ribosomes. The plastid genomes of seed plants contain a conserved set of ribosomal protein genes. Three of these have proven to be nonessential for translation and, thus, for cellular viability: rps15, rpl33, and rpl36. To help define the minimum ribosome, here, we examined whether more than one of these nonessential plastid ribosomal proteins can be removed from the 70S ribosome. To that end, we constructed all possible double knockouts for the S15, L33, and L36 ribosomal proteins by stable transformation of the tobacco (Nicotiana tabacum) plastid genome. We find that, although S15 and L33 function in different ribosomal particles (30S and 50S, respectively), their combined deletion from the plastid genome results in synthetic lethality under autotrophic conditions. Interestingly, the lethality can be overcome by growth under elevated temperatures due to an improved efficiency of plastid ribosome biogenesis. Our results reveal functional interactions between protein and RNA components of the 70S ribosome and uncover the interdependence of the biogenesis of the two ribosomal subunits. In addition, our findings suggest that defining a minimal set of plastid genes may prove more complex than generally believed.

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“…First, we confirmed the essentiality of rpsU and rpsK for cell growth. We successfully created a mutant in which the rpsU-yqeY operon was deleted by replacing these two open reading frames with an antibiotic-resistance cassette (NBS1513); however, compared to a previous study, 31) rpsK was not deleted in this mutant. We concluded that rpsK but not rpsU was essential for cell growth using rpsK-and rpsU-inducible strains (NBS1533 and NBS1530, Supplemental Fig.…”

Section: Resultsmentioning

confidence: 99%

Cell motility and biofilm formation in Bacillus subtilis are affected by the ribosomal proteins, S11 and S21

Takada

Morita

Shiwa

et al. 2014

Bioscience, Biotechnology, and Biochemistry

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Bacillus subtilis differentiates into various cellular states in response to environmental changes. It exists in two states during the exponential growth phase: motile cells and connected chains of sessile cells. Here, we identified new regulators of cell motility and chaining, the ribosomal proteins S21 (rpsU) and S11 (rpsK). Their mutants showed impaired cell motility (observed in a laboratory strain) and robust biofilm formation (observed in an undomesticated strain). The two major operons for biofilm formation, tapA-sipW-tasA and epsA-O, were strongly expressed in the rpsU mutant, whereas the flagellin-encoding hag gene and other SigD-dependent motility regulons were not. Genetic analysis revealed that the mutation of remA, the transcriptional activator of the eps operon, is epistatic to that of rpsU, whereas the mutation of antagonistic regulators of SinR is not. Our studies demonstrate that S11 and S21 participate in the regulation of bistability via the RemA/RemB pathway.

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Inactivation of Ribosomal Protein Genes in Bacillus subtilis Reveals Importance of Each Ribosomal Protein for Cell Proliferation and Cell Differentiation

Cited by 92 publications

References 64 publications

Multiple rRNA operons are essential for efficient cell growth and sporulation as well as outgrowth in Bacillus subtilis

Multiple rRNA operons are essential for efficient cell growth and sporulation as well as outgrowth in Bacillus subtilis

Synthetic Lethality in the Tobacco Plastid Ribosome and Its Rescue at Elevated Growth Temperatures

Cell motility and biofilm formation in Bacillus subtilis are affected by the ribosomal proteins, S11 and S21

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