Control of ribosome synthesis in bacteria: the important role of rRNA chain elongation rate
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ntrol of ribosome synthesis in bacteria: the important role of rRNA chain elongation rate *
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Manlu Zhu , Haoyan Mu , Mengmei Jia , Lingfu Deng & Xiongfeng Dai
Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University, Wuhan 430079, China Received March 9, 2020; accepted May 26, 2020; published online August 20, 2020
Bacteria growth depends crucially on protein synthesis, which is limited by ribosome synthesis. Ribosomal RNA (rRNA) transcription is the rate-limiting step of ribosome synthesis. It is generally proposed that the transcriptional initiation rate of rRNA operon is the primary factor that controls the rRNA synthesis. In this study, we established a convenient GFP-based reporter approach for measuring the bacterial rRNA chain elongation rate. We showed that the rRNA chain elongation rate of Escherichia coli remains constant under nutrient limitation and chloramphenicol inhibition. In contrast, rRNA chain elongation rate decreases dramatically under low temperatures. Strikingly, we found that Vibrio natriegens, the fastest growing bacteria known, has a 50% higher rRNA chain elongation rate than E. coli, which contributes to its rapid ribosome synthesis. Our study demonstrates that rRNA chain elongation rate is another important factor that affects the bacterial ribosome synthesis capacity. rRNA chain elongation rate, ribosome synthesis, rrn transcriptional initiation rate, GFP reporter system, low temperature, Vibrio natriegens Citation:
Zhu, M., Mu, H., Jia, M., Deng, L., and Dai, X. (2020). Control of ribosome synthesis in bacteria: the important role of rRNA chain elongation rate. Sci China Life Sci 63, https://doi.org/10.1007/s11427-020-1742-4
INTRODUCTION Growth is the core property of bacterial cells. Protein accounts for over half of bacterial cellular biomass, and its synthesis consumes 70% of the total cellular energy budget (Basan et al., 2015; Klumpp et al., 2013; Zhu and Dai, 2018). Therefore, protein synthesis lies at the core of bacterial growth. Rapid cell growth and high protein synthesis rate require highly abundant ribosome content. The important role of ribosome synthesis in bacterial cell growth is strongly indicated by the linear correlation between the ribosome content and growth rate under different nutrient conditions (Dai et al., 2016; Scott et al., 2010). The ribosome synthesis rate of E. coli varies over 20-fold under different nutrient *Corresponding authors (Manlu Zhu, email: [email protected]; Xiongfeng Dai, email: [email protected]) †Contributed equally to this work
conditions (doubling time ranges from ~20 min to several hours) (Bremer and Dennis, 1996; Gourse et al., 1996; Scott et al., 2014). Mechanistically, the bacterial ribosome synthesis is primarily limited by (p)ppGpp-controlled rRNA synthesis since the synthesis of ribosomal protein (r-protein) is coordinated with rRNA synthesis via autogenous feedback control. Specific regulatory r-proteins bind to the leader regions o
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