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The DEAD-Box RNA Helicases of Bacillus subtilis as a Model to Evaluate Genetic Compensation Among Duplicate Genes.

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 ?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 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 ?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.

SUBMITTER: Gonzalez-Gutierrez JA

PROVIDER: S-EPMC6178137 | biostudies-other | 2018

REPOSITORIES: biostudies-other

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The DEAD-Box RNA Helicases of Bacillus subtilis as a Model to Evaluate Genetic Compensation Among Duplicate Genes.

González-Gutiérrez José Antonio JA Díaz-Jiménez Diana Fabiola DF Vargas-Pérez Itzel I Guillén-Solís Gabriel G Stülke Jörg J Olmedo-Álvarez Gabriela G

Frontiers in microbiology 20180925

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 c ...[more]

PMID: 30337909

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Project description:Although RNA helicases are essentially ubiquitous and perform roles in all stages of RNA metabolism, phylogenetic analysis of the DEAD (Asp-Glu-Ala-Asp)-box RNA helicase family in a single phylum has not been performed. Here, we performed a phylogenetic analysis on DEAD-box helicases from all currently available cyanobacterial genomes, comprising a total of 362 helicase protein sequences from 280 strains. DEAD-box helicases belonging to three distinct clades were observed. Two clades, the CsdA (cold shock DEAD-box A)-like and RhlE (RNA helicase E)-like helicases, cluster with the homologous proteins from Escherichia coli. The third clade, the CrhR (cyanobacterial RNA helicase Redox)-like helicases, is unique to cyanobacteria and characterized by a conserved sequence motif in the C-terminal extension. Restricted distribution is observed across cyanobacterial diversity with respect to both helicase type and strain. CrhR-like and CsdA-like helicases essentially never occur together, while RhlE always occurs with either a CrhR-like or CsdA-like helicase. CrhR-like and RhlE-like proteins occurred in filamentous cyanobacteria of the orders Nostocales, Oscillatoriales and Synechococcales. Similarly, CsdA- and RhlE-like proteins are restricted to unicellular cyanobacteria of the genera Cyanobium and Synechococcus. In addition, the unexpected occurrence of RhlE in two Synechococcus strains suggests recent acquisition and evolutionary divergence. This study, therefore, raises physiological and evolutionary questions as to why DEAD-box RNA helicases encoded in cyanobacterial lineages display restricted distributions, suggesting niches that require either CrhR or CsdA RNA helicase activity but not both. Extensive conservation of gene synteny surrounding the previously described rimO-crhR operon is also observed, indicating a role in the maintenance of photosynthesis. The analysis provides insights into the evolution, origin and dissemination of sequences within a single gene family to yield divergent functional roles.

Dataset Information

The DEAD-Box RNA Helicases of Bacillus subtilis as a Model to Evaluate Genetic Compensation Among Duplicate Genes.

Publications

The DEAD-Box RNA Helicases of <i>Bacillus subtilis</i> as a Model to Evaluate Genetic Compensation Among Duplicate Genes.

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