Abstract
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°C, and all single deletion mutants exhibit defective growth at 18°C except for ΔdeaD/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 superfamily 2 (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 ΔyfmL 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.
Highlights
In bacteria, up to 44% of genes could come from duplication (Zhang, 2003; Hannay et al, 2008; Serres et al, 2009)
We explored whether in B. subtilis the absence of a phenotype under some conditions in single DEAD-box RNA helicases (DBRH) deletion mutants (Lehnik-Habrink et al, 2013), could be explained by the redundancy afforded by the conserved helicase superfamily 2 (SF2) core in the different paralogs
Since the B. subtilis DBRH perform specific roles in ribosome biogenesis and RNA degradation (Ando and Nakamura, 2006; Kossen et al, 2002; Lehnik-Habrink et al, 2013) and, as we show in this study, they do not complement each other it is intriguing that none of them is essential for growth
Summary
Up to 44% of genes could come from duplication (Zhang, 2003; Hannay et al, 2008; Serres et al, 2009). Most of the duplicated genes appear to result from gene duplication events, probably in response to different selection pressures, such as starvation conditions and physical stress It is unclear how duplicate genes transit from an initial state of redundancy. Redundancy is frequently associated with paralogs that share an identical biochemical function (Prince and Pickett, 2002). It explains a buffering relationship where genes can compensate for each other’s loss by their ability to share and takeover the same function. In this manner, genetic buffering results in the masking of the phenotypic consequences of mutations (Hartman et al, 2001; Thomaides et al, 2007). As DeLuna et al (2008) suggest “functional overlap between paralogs explains the individual dispensability of most genes that are duplicated in Saccharomyces cerevisiae.”
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