RNase AM, a 5' to 3' Exonuclease, Matures the 5' End of All Three Ribosomal RNAs in E. Coli

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2020 Apr 29

PMID 32343306

Citations 12

Authors

Chaitanya Jain

Affiliations

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Abstract

Bacterial ribosomal RNAs (rRNAs) are transcribed as precursors and require processing by Ribonucleases (RNases) to generate mature and functional rRNAs. Although the initial steps of rRNA processing in Escherichia coli (E. coli) were described several decades ago, the enzymes responsible for the final steps of 5S and 23S rRNA 5'-end maturation have remained unknown. Here, I show that RNase AM, a recently identified 5' to 3' exonuclease, performs the last step of 5S rRNA 5'-end maturation. RNase AM was also found to generate the mature 5' end of 23S rRNA, subsequent to a newly identified prior processing step. Additionally, RNase AM was found to mature the 5' end of 16S rRNA, a reaction previously attributed to RNase G. These findings indicate a major role for RNase AM in cellular RNA metabolism and establish a biological role for the first 5' to 3' RNA exonuclease identified in E. coli.

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References

Ghodge S, Raushel F . Discovery of a Previously Unrecognized Ribonuclease from Escherichia coli That Hydrolyzes 5'-Phosphorylated Fragments of RNA. Biochemistry. 2015; 54(18):2911-8. DOI: 10.1021/acs.biochem.5b00192. View

Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M . Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006; 2:2006.0008. PMC: 1681482. DOI: 10.1038/msb4100050. View

Smith B, Gupta N, Denny K, Culver G . Characterization of 16S rRNA Processing with Pre-30S Subunit Assembly Intermediates from E. coli. J Mol Biol. 2018; 430(12):1745-1759. DOI: 10.1016/j.jmb.2018.04.009. View

Redko Y, Bechhofer D, Condon C . Mini-III, an unusual member of the RNase III family of enzymes, catalyses 23S ribosomal RNA maturation in B. subtilis. Mol Microbiol. 2008; 68(5):1096-106. DOI: 10.1111/j.1365-2958.2008.06207.x. View

Condon C, Rourera J, Brechemier-Baey D, Putzer H . Ribonuclease M5 has few, if any, mRNA substrates in Bacillus subtilis. J Bacteriol. 2002; 184(10):2845-9. PMC: 135035. DOI: 10.1128/JB.184.10.2845-2849.2002. View

Britton R, Wen T, Schaefer L, Pellegrini O, Uicker W, Mathy N . Maturation of the 5' end of Bacillus subtilis 16S rRNA by the essential ribonuclease YkqC/RNase J1. Mol Microbiol. 2007; 63(1):127-38. DOI: 10.1111/j.1365-2958.2006.05499.x. View

Piir K, Paier A, Liiv A, Tenson T, Maivali U . Ribosome degradation in growing bacteria. EMBO Rep. 2011; 12(5):458-62. PMC: 3090016. DOI: 10.1038/embor.2011.47. View

Bram R, Young R, Steitz J . The ribonuclease III site flanking 23S sequences in the 30S ribosomal precursor RNA of E. coli. Cell. 1980; 19(2):393-401. DOI: 10.1016/0092-8674(80)90513-9. View

Ehrenberg M, Bremer H, Dennis P . Medium-dependent control of the bacterial growth rate. Biochimie. 2012; 95(4):643-58. DOI: 10.1016/j.biochi.2012.11.012. View

10.

Nomura M, Gourse R, Baughman G . Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem. 1984; 53:75-117. DOI: 10.1146/annurev.bi.53.070184.000451. View

11.

Jain C . Role of ribosome assembly in Escherichia coli ribosomal RNA degradation. Nucleic Acids Res. 2018; 46(20):11048-11060. PMC: 6237783. DOI: 10.1093/nar/gky808. View

12.

Li Z, Pandit S, Deutscher M . RNase G (CafA protein) and RNase E are both required for the 5' maturation of 16S ribosomal RNA. EMBO J. 1999; 18(10):2878-85. PMC: 1171368. DOI: 10.1093/emboj/18.10.2878. View

13.

Kiss A, Sain B, VENETIANER P . The number of rRNA genes in Escherichia coli. FEBS Lett. 1977; 79(1):77-9. DOI: 10.1016/0014-5793(77)80354-2. View

14.

Young R, Steitz J . Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc Natl Acad Sci U S A. 1978; 75(8):3593-7. PMC: 392831. DOI: 10.1073/pnas.75.8.3593. View

15.

Li Z, Deutscher M . The tRNA processing enzyme RNase T is essential for maturation of 5S RNA. Proc Natl Acad Sci U S A. 1995; 92(15):6883-6. PMC: 41434. DOI: 10.1073/pnas.92.15.6883. View

16.

Diwa A, BRICKER A, Jain C, Belasco J . An evolutionarily conserved RNA stem-loop functions as a sensor that directs feedback regulation of RNase E gene expression. Genes Dev. 2000; 14(10):1249-60. PMC: 316614. View

17.

Bechhofer D, Deutscher M . Bacterial ribonucleases and their roles in RNA metabolism. Crit Rev Biochem Mol Biol. 2019; 54(3):242-300. PMC: 6776250. DOI: 10.1080/10409238.2019.1651816. View

18.

Jagessar K, Jain C . Functional and molecular analysis of Escherichia coli strains lacking multiple DEAD-box helicases. RNA. 2010; 16(7):1386-92. PMC: 2885687. DOI: 10.1261/rna.2015610. View

19.

Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H . Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 2006; 12(5):291-9. DOI: 10.1093/dnares/dsi012. View

20.

Wachi M, Umitsuki G, Shimizu M, Takada A, Nagai K . Escherichia coli cafA gene encodes a novel RNase, designated as RNase G, involved in processing of the 5' end of 16S rRNA. Biochem Biophys Res Commun. 1999; 259(2):483-8. DOI: 10.1006/bbrc.1999.0806. View