Quality Control by Isoleucyl-tRNA Synthetase of Bacillus subtilis Is Required for Efficient Sporulation

被引:13
作者
Kermgard, Elizabeth [1 ,7 ]
Yang, Zhou [1 ]
Michel, Annika-Marisa [1 ,2 ]
Simari, Rachel [3 ]
Wong, Jacqueline [1 ]
Ibba, Michael [3 ,4 ,5 ]
Lazazzera, Beth A. [1 ,6 ]
机构
[1] Univ Calif Los Angeles, Dept Microbiol Immunol & Mol Genet, Los Angeles, CA 90095 USA
[2] Tech Univ Carolo Wilhelmina Braunschweig, Inst Microbiol, Braunschweig, Germany
[3] Ohio State Univ, Ohio State Biochem Program, Columbus, OH 43210 USA
[4] Ohio State Univ, Dept Microbiol, 484 W 12th Ave, Columbus, OH 43210 USA
[5] Ohio State Univ, Ctr RNA Biol, Columbus, OH 43210 USA
[6] Univ Calif Los Angeles, Mol Biol Inst, Los Angeles, CA 90095 USA
[7] St Louis Univ, Sch Med, St Louis, MO 63104 USA
基金
美国国家科学基金会;
关键词
MISACTIVATED AMINO-ACID; TO-SITE TRANSLOCATION; GENETIC-CODE; MASTER REGULATOR; EDITING ACTIVITY; CP1; DOMAIN; INITIATION; TRANSCRIPTION; MECHANISMS; EXPRESSION;
D O I
10.1038/srep41763
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Isoleucyl-tRNA synthetase (IleRS) is an aminoacyl-tRNA synthetase whose essential function is to aminoacylate tRNA(Ile) with isoleucine. Like some other aminoacyl-tRNA synthetases, IleRS can mischarge tRNA(Ile) and correct this misacylation through a separate post-transfer editing function. To explore the biological significance of this editing function, we created a ileS(T233P) mutant of Bacillus subtilis that allows tRNA(Ile) mischarging while retaining wild-type Ile-tRNA(Ile) synthesis activity. As seen in other species defective for aminoacylation quality control, the growth rate of the ileS(T233P) strain was not significantly different from wild-type. When the ileS(T233P) strain was assessed for its ability to promote distinct phenotypes in response to starvation, the ileS(T233P) strain was observed to exhibit a significant defect in formation of environmentally resistant spores. The sporulation defect ranged from 3-fold to 30-fold and was due to a delay in activation of early sporulation genes. The loss of aminoacylation quality control in the ileS(T233P) strain resulted in the inability to compete with a wild-type strain under selective conditions that required sporulation. These data show that the quality control function of IleRS is required in B. subtilis for efficient sporulation and suggests that editing by aminoacyl-tRNA synthetases may be important for survival under starvation/nutrient limitation conditions.
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页数:9
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共 68 条
[1]   The SpollE phosphatase, the sporulation septum and the establishment of forespore-specific transcription in Bacillus subtilis:: a reassessment [J].
Arigoni, F ;
Guérout-Fleury, AM ;
Barák, I ;
Stragier, P .
MOLECULAR MICROBIOLOGY, 1999, 31 (05) :1407-1415
[2]   Genetic code ambiguity confers a selective advantage on Acinetobacter baylyi [J].
Bacher, Jamie A. ;
Waas, William F. ;
Metzgar, David ;
de Crecy-Lagard, Valerie ;
Schimmel, Paul .
JOURNAL OF BACTERIOLOGY, 2007, 189 (17) :6494-6496
[3]   An editing-defective aminoacyl-tRNA synthetase is mutagenic in aging bacteria via the SOS response [J].
Bacher, Jamie M. ;
Schimmel, Paul .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (06) :1907-1912
[4]   Inhibited cell growth and protein functional changes from an editing-defective tRNA synthetase [J].
Bacher, JM ;
de Crécy-Lagard, V ;
Schimmel, PR .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (05) :1697-1701
[5]   Interstice mutations that block site-to-site translocation of a misactivated amino acid bound to a class I tRNA synthetase [J].
Bishop, AC ;
Beebe, K ;
Schimmel, PR .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2003, 100 (02) :490-494
[6]   Blocking site-to-site translocation of a misactivated amino acid by mutation of a class I tRNA synthetase [J].
Bishop, AC ;
Nomanbhoy, TK ;
Schimmel, P .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2002, 99 (02) :585-590
[7]   Translation quality control is critical for bacterial responses to amino acid stress [J].
Bullwinkle, Tammy J. ;
Ibba, Michael .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2016, 113 (08) :2252-2257
[8]   Oxidation of cellular amino acid pools leads to cytotoxic mistranslation of the genetic code [J].
Bullwinkle, Tammy J. ;
Reynolds, Noah M. ;
Raina, Medha ;
Moghal, Adil ;
Matsa, Eleftheria ;
Rajkovic, Andrei ;
Kayadibi, Huseyin ;
Fazlollahi, Farbod ;
Ryan, Christopher ;
Howitz, Nathaniel ;
Faull, Kym F. ;
Lazazzera, Beth A. ;
Ibba, Michael .
ELIFE, 2014, 3
[9]   Broadly heterogeneous activation of the master regulator for sporulation in Bacillus subtilis [J].
Chastanet, Arnaud ;
Vitkup, Dennis ;
Yuan, Guo-Cheng ;
Norman, Thomas M. ;
Liu, Jun S. ;
Losick, Richard M. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (18) :8486-8491
[10]   Glutamyl-tRNAGln amidotransferase in Deinococcus radiodurans may be confined to asparagine biosynthesis [J].
Curnow, AW ;
Tumbula, DL ;
Pelaschier, JT ;
Min, B ;
Söll, D .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1998, 95 (22) :12838-12843