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Front. Microbiol. | doi: 10.3389/fmicb.2018.02261

The DEAD-box RNA helicases of Bacillus subtilis as a model to evaluate genetic compensation among duplicate genes

  • 1Ingeniería Genetica, Unidad Irapuato (CINVESTAV), Mexico
  • 2Biologia molecular de plantas, National Autonomous University of Mexico (Morelos), Mexico
  • 3Institute for Microbiology and Genetics, Georg-August-Universität Göttingen, Germany

The presence of duplicated genes in organisms is well documented. There is increasing interest in understanding how these genes subfunctionalize and whether functional overlap can explain the fact that some of these genes are dispensable. Bacillus subtilis possesses four DEAD-box RNA helicases (DBRH) genes, cshA, cshB, deaD/yxiN, and yfmL that make a good case to study to what extent they can complement each other despite their subfunctionalization. They possess the highly conserved N-terminal catalytic domain core common to RNA helicases, but different carboxy-terminal ends. All four genes have been shown to have independent functions although all participate in rRNA assembly. None of the B. subtilis DBRH is essential for growth at 37 oC, and all single deletion mutants exhibit defective growth at 18 oC except for deaD/yxiN. Evaluation of double mutants did not reveal negative epistasis, suggesting that they do not have overlapping functions. The absence of any one gene distorts the expression pattern of the others, but not in a specific pattern suggestive of compensation. Overexpression of these paralogous genes in the different mutant backgrounds did not result in cross-complementation, further confirming their lack of buffering capability. Since no complementation could be observed among full sized proteins, we evaluated to what extent the SF2 helicase core of the smallest DBRH, YfmL, could be functional when hooked to each of the C-terminal end of CshA, CshB, and DeaD/YxiN. None of the different chimeras complemented the different mutants, and instead, all chimeras inhibited the growth of the ∆yfmL mutant, and other combinations were also deleterious. Our findings suggest that the long time divergence between DEAD-box RNA helicase genes has resulted in specialized activities in RNA metabolism and shows that these duplicated genes cannot buffer one another.

Keywords: Paralogues, DEAD-box RNA Helicases, Epistasis, Bacillus subtilis, genetic interactions, Duplicated genes

Received: 06 Jun 2017; Accepted: 05 Sep 2018.

Edited by:

Ludmila Chistoserdova, University of Washington, United States

Reviewed by:

Hala Chamieh, Lebanese University, Lebanon
Edward Bolt, University of Nottingham, United Kingdom  

Copyright: © 2018 González-Gutiérrez, Diaz-Jimenez, Vargas-Peréz, Guillen-Solis, Stülke and Olmedo-Alvarez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Gabriela Olmedo-Alvarez, Unidad Irapuato (CINVESTAV), Ingeniería Genetica, Irapuato, 36821, Guanajuato, Mexico,