Translational GTPase BipA Is Involved in the Maturation of a Large Subunit of Bacterial Ribosome at Suboptimal Temperature

Goh, Kwok Jian; Ero, Rya; Yan, Xin-Fu; Park, Jung-Eun; Kundukad, Binu; Zheng, Jun; Sze, Siu Kwan; Gao, Yong‐Gui

doi:10.3389/fmicb.2021.686049

Cited by 8 publications

(4 citation statements)

References 65 publications

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“…To the contrary, at 20°C, ESC19 cells harboring pACYC184 showed a significant reduction in 70S ribosomes and accumulation of free ribosomal subunits (right panel in Figure 5A ). In addition, an abnormal peak was observed between the two ribosomal subunits (red arrowheads in Figure 5A ), which is consistent with previous studies ( Choi and Hwang, 2018 ; Gibbs and Fredrick, 2018 ; Goh et al, 2021 ). This profile was also observed in the cells transformed with pBIS05-2.…”

Section: Resultssupporting

confidence: 92%

“…In the subunit profiles of ESC19 cells with pBIS02-2 and pBIS07-1, only a single precursor particle appeared adjacent to the 50S ribosomal subunit peak, with increased normal 50S ribosomal subunits (red arrowhead in Figure 5B ). ( Goh et al, 2021 ) Based on these findings, we confirmed that YebC could not resolve ribosomal defects in the strain ESC19. Notably, ESC19 cells expressing either L20 or NhaR exhibited almost identical polysome and subunit profiles, implying that suppressive NhaR may be able to promote ribosome biogenesis at low temperature.…”

Section: Resultssupporting

confidence: 63%

“…7 nt at 5′and 7–9 nt at 3′ends of pre-23S rRNA sequence and 115 nt at 5′and 33 nt at 3′ends of pre-16S rRNA are removed to produce mature forms ( Young and Steitz, 1978 ; King et al, 1986 ) ( Supplementary Figure S5 ). It was also reported that the deletion of bipA leads to the accumulation of rRNA precursors ( Choi et al, 2020b ), and upregulation of ribosome maturation factors such as DeaD and RNase R ( Goh et al, 2021 ). Therefore, to investigate whether NhaR restores rRNA processing in ESC19, rRNA from ESC19 cells harboring pACYC184, pACYC184BipA, pBIS02-2, or pBIS07-1 were analyzed by Northern blotting.…”

Section: Resultsmentioning

confidence: 99%

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Novel rRNA transcriptional activity of NhaR revealed by its growth recovery for the bipA-deleted Escherichia coli at low temperature

Choi

Huh

Hwang

2023

Front. Mol. Biosci.

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The BipA protein is a universally conserved GTPase in bacterial species and is structurally similar to translational GTPases. Despite its wide distribution, BipA is dispensable for growth under optimal growth conditions but is required under stress conditions. In particular, bipA-deleted cells (ESC19) have been shown to display a variety of phenotypic changes in ribosome assembly, capsule production, lipopolysaccharide (LPS) synthesis, biofilm formation, and motility at low temperature, suggesting its global regulatory roles in cold adaptation. Here, through genomic library screening, we found a suppressor clone containing nhaR, which encodes a Na+-responsive LysR-type transcriptional regulator and whose gene product partially restored the growth of strain ESC19 at 20°C. The suppressed cells showed slightly reduced capsule production and improved biofilm-forming ability at 20°C, whereas the defects in the LPS core and swimming motility were not restored but aggravated by overexpression of nhaR. Notably, the overexpression partially alleviated the defects in 50S ribosomal subunit assembly and rRNA processing of ESC19 cells by enhancing the overall transcription of rRNA. Electrophoretic mobility shift assay revealed the association of NhaR with the promoter of seven rrn operons, suggesting that NhaR directly regulates rRNA transcription in ESC19 at 20°C. The suppressive effects of NhaR on ribosomes, capsules, and LPS were dependent on its DNA-binding activity, implying that NhaR might be a transcriptional factor involved in regulating these genes at 20°C. Furthermore, we found that BipA may be involved in adaptation to salt stress, designating BipA as a global stress-responsive regulator, as the deletion of bipA led to growth defects at 37°C and high Na+ concentrations without ribosomal defects.

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Section: Resultssupporting

confidence: 92%

Section: Resultssupporting

confidence: 63%

Section: Resultsmentioning

confidence: 99%

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Novel rRNA transcriptional activity of NhaR revealed by its growth recovery for the bipA-deleted Escherichia coli at low temperature

Choi

Huh

Hwang

2023

Front. Mol. Biosci.

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“…Era is an essential protein and is one of the multiple ribosome-associated GTPases (RA-GTPases). In addition to Era, RA-GTPases such as RsgA, Der, BipA, and ObgE function in various stages of the ribosome assembly process ( Britton, 2009 ; Gibbs et al, 2020 ; Goh et al, 2021 ). Era binds near the 3′ end of the 16S rRNA of the 30S subunit ( Sayed et al, 1999 ; Tu et al, 2009 , 2011 ).…”

Section: Introductionmentioning

confidence: 99%

A Mutant Era GTPase Suppresses Phenotypes Caused by Loss of Highly Conserved YbeY Protein in Escherichia coli

et al. 2022

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Ribosome assembly is a complex fundamental cellular process that involves assembling multiple ribosomal proteins and several ribosomal RNA species in a highly coordinated yet flexible and resilient manner. The highly conserved YbeY protein is a single-strand specific endoribonuclease, important for ribosome assembly, 16S rRNA processing, and ribosome quality control. In Escherichia coli, ybeY deletion results in pleiotropic phenotypes including slow growth, temperature sensitivity, accumulation of precursors of 16S rRNA, and impaired formation of fully assembled 70S subunits. Era, an essential highly conserved GTPase protein, interacts with many ribosomal proteins, and its depletion results in ribosome assembly defects. YbeY has been shown to interact with Era together with ribosomal protein S11. In this study, we have analyzed a suppressor mutation, era(T99I), that can partially suppress a subset of the multiple phenotypes of ybeY deletion. The era(T99I) allele was able to improve 16S rRNA processing and ribosome assembly at 37°C. However, it failed to suppress the temperature sensitivity and did not improve 16S rRNA stability. The era(T99I) allele was also unable to improve the 16S rRNA processing defects caused by the loss of ribosome maturation factors. We also show that era(T99I) increases the GroEL levels in the 30S ribosome fractions independent of YbeY. We propose that the mechanism of suppression is that the changes in Era’s structure caused by the era(T99I) mutation affect its GTP/GDP cycle in a way that increases the half-life of RNA binding to Era, thereby facilitating alternative processing of the 16S RNA precursor. Taken together, this study offers insights into the role of Era and YbeY in ribosome assembly and 16S rRNA processing events.

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Bacterial GTPases as druggable targets to tackle antimicrobial resistance

Shanbhag

Saraogi

2023

Bioorganic & Medicinal Chemistry Letters

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Translational GTPase BipA Is Involved in the Maturation of a Large Subunit of Bacterial Ribosome at Suboptimal Temperature

Cited by 8 publications

References 65 publications

Novel rRNA transcriptional activity of NhaR revealed by its growth recovery for the bipA-deleted Escherichia coli at low temperature

Novel rRNA transcriptional activity of NhaR revealed by its growth recovery for the bipA-deleted Escherichia coli at low temperature

A Mutant Era GTPase Suppresses Phenotypes Caused by Loss of Highly Conserved YbeY Protein in Escherichia coli

Bacterial GTPases as druggable targets to tackle antimicrobial resistance

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