A Bias in the Reading of the Genetic Code of Escherichia coli is a Characteristic for Genes that Specify Stress-induced MazF-mediated Proteins

Author(s): Akanksha Nigam, Adi Oron-Gottesman, Hanna Engelberg-Kulka*

Journal Name: Current Genomics

Volume 21 , Issue 4 , 2020

Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Background: Escherichia coli (E. coli) mazEF, a stress-induced toxin-antitoxin (TA) system, has been studied extensively. The MazF toxin is an endoribonuclease that cleaves RNAs at ACA sites. Thereby, under stress, the induced MazF generates a Stress-induced Translation Machinery (STM), composed of MazF processed mRNAs and selective ribosomes that specifically translate the processed mRNAs.

Materials and Methods: Based on the data from the EcoCyc website of the National Center for Biotechnology Information (NCBI), the sequence of all E. coli MG1655 genes were scanned for ACA sites upstream from the initiation codons. Among these sequences, the fuzznuc program of the "European Molecular Biology Open Software Suite" (EMBOSS) was used to find the "ACA" pattern. The distribution of the ACA threonine codon, both in-frame and out-of-frame, was determined by using the HTML Script Program (Supplementary Material).

Results: Here it is reported that for most of the E. coli proteins mediated by stress-induced MazF, the ACA threonine codon in their mRNAs is not in-frame but rather out-of-frame; in these same RNAs, the three synonymous threonine codons, ACG, ACU, and ACC, are in-frame. In contrast, for proteins translated by the canonical translation system, in the majority of mRNAs, the ACA codon is located in-frame.

Conclusion: The described bias in the genetic code is a characteristic of E. coli genes specifying for stress-induced MazF-mediated proteins.

Keywords: Genetic code, Toxin-Antitoxin (TA) modules, E. coli, MazF toxin, ACA sites, genes.

Aizenman, E.; Engelberg-Kulka, H.; Glaser, G. An Escherichia coli chromosomal “addiction module” regulated by guanosine [corrected 3′,5′-bispyrophosphate: a model for programmed bacterial cell death. Proc. Natl. Acad. Sci. USA, 1996, 93(12), 6059-6063.
[http://dx.doi.org/10.1073/pnas.93.12.6059] [PMID: 8650219]
Engelberg-Kulka, H.; Glaser, G. Addiction modules and programmed cell death and antideath in bacterial cultures. Annu. Rev. Microbiol., 1999, 53, 43-70.
[http://dx.doi.org/10.1146/annurev.micro.53.1.43] [PMID: 10547685]
Mittenhuber, G. Occurrence of mazEF-like antitoxin/toxin systems in bacteria. J. Mol. Microbiol. Biotechnol., 1999, 1(2), 295-302.
[PMID: 10943559]
Pandey, D.P.; Gerdes, K. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res., 2005, 33(3), 966-976.
[http://dx.doi.org/10.1093/nar/gki201] [PMID: 15718296]
Hazan, R.; Sat, B.; Engelberg-Kulka, H. Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J. Bacteriol., 2004, 186(11), 3663-3669.
[http://dx.doi.org/10.1128/JB.186.11.3663-3669.2004] [PMID: 15150257]
Godoy, V.G.; Jarosz, D.F.; Walker, F.L.; Simmons, L.A.; Walker, G.C. Y-family DNA polymerases respond to DNA damage-independent inhibition of replication fork progression. EMBO J., 2006, 25(4), 868-879.
[http://dx.doi.org/10.1038/sj.emboj.7600986] [PMID: 16482223]
Sat, B.; Hazan, R.; Fisher, T.; Khaner, H.; Glaser, G.; Engelberg-Kulka, H. Programmed cell death in Escherichia coli: some antibiotics can trigger mazEF lethality. J. Bacteriol., 2001, 183(6), 2041-2045.
[http://dx.doi.org/10.1128/JB.183.6.2041-2045.2001] [PMID: 11222603]
Zhang, Y.; Zhang, J.; Hoeflich, K.P.; Ikura, M.; Qing, G.; Inouye, M.; Maz, F. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol. Cell, 2003, 12(4), 913-923.
[http://dx.doi.org/10.1016/S1097-2765(03)00402-7] [PMID: 14580342]
Zhang, Y.; Zhang, J.; Hara, H.; Kato, I.; Inouye, M. Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase. J. Biol. Chem., 2005, 280(5), 3143-3150.
[http://dx.doi.org/10.1074/jbc.M411811200] [PMID: 15537630]
Vesper, O.; Amitai, S.; Belitsky, M.; Byrgazov, K.; Kaberdina, A.C.; Engelberg-Kulka, H.; Moll, I. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell, 2011, 147(1), 147-157.
[http://dx.doi.org/10.1016/j.cell.2011.07.047] [PMID: 21944167]
Sauert, M.; Wolfinger, M.T.; Vesper, O.; Müller, C.; Byrgazov, K.; Moll, I. The MazF-regulon: a toolbox for the post-transcriptional stress response in Escherichia coli. Nucleic Acids Res., 2016, 44(14), 6660-6675.
[http://dx.doi.org/10.1093/nar/gkw115] [PMID: 26908653]
Moll, I.; Engelberg-Kulka, H. Selective translation during stress in Escherichia coli. Trends Biochem. Sci., 2012, 37(11), 493-498.
[http://dx.doi.org/10.1016/j.tibs.2012.07.007] [PMID: 22939840]
Nigam, A.; Ziv, T.; Oron-Gottesman, A.; Engelberg-Kulka, H. Stress-induced MazF-mediated proteins in Escherichia coli. MBio, 2019, 10(2), e00340-e19.
[http://dx.doi.org/10.1128/mBio.00340-19] [PMID: 30914510]
Oron-Gottesman, A.; Sauert, M.; Moll, I.; Engelberg-Kulka, H. A Stress-induced bias in the reading of the genetic code in Escherichia coli. MBio, 2016, 7(6), e01855-e16.
[http://dx.doi.org/10.1128/mBio.01855-16] [PMID: 27935840]
Aoi, R.; Miyamoto, T.; Yokota, A.; Ota, Y.; Fujitani, H.; Tsuneda, S.; Noda, N.; Maz, F. MazF endoribonucleolytic toxin conserved in Nitrospira specifically cleaves the AACU, AACG, and AAUU motifs. Toxins (Basel), 2020, 12(5)E287
[http://dx.doi.org/10.3390/toxins12050287] [PMID: 32365819]
Rice, P.; Longden, I.; Bleasby, A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet., 2000, 16(6), 276-277.
[http://dx.doi.org/10.1016/S0168-9525(00)02024-2] [PMID: 10827456]

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2020
Published on: 08 August, 2020
Page: [311 - 318]
Pages: 8
DOI: 10.2174/1389202921999200606215305
Price: $65

Article Metrics

PDF: 12
PRC: 1