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A novel three-unit tRNA splicing endonuclease found in ultrasmall Archaea possesses broad substrate specificity

Journal Article · · Nucleic Acids Research
DOI:https://doi.org/10.1093/nar/gkr692· OSTI ID:1904531
 [1];  [2];  [3];  [3];  [4];  [2];  [2];  [2];  [3];  [2]
  1. Keio University, Tsuruoka (Japan); Keio Univ., Tsuruoka (Japan)
  2. Keio University, Tsuruoka (Japan)
  3. University of California, Berkeley, CA (United States)
  4. Institute of Genetics and Biophysics ‘Adriano Buzzati Traverso, Naples (Italy)
+ Show Author Affiliations
tRNA splicing endonucleases, essential enzymes found in Archaea and Eukaryotes, are involved in the processing of pre-tRNA molecules. In Archaea, three types of splicing endonuclease [homotetrameric: α4, homodimeric: α2, and heterotetrameric: (αβ)2] have been identified, each representing different substrate specificity during the tRNA intron cleavage. Here, we discovered a fourth type of archaeal tRNA splicing endonuclease (ε2) in the genome of the acidophilic archaeon Candidatus Micrarchaeum acidiphilum, referred to as ARMAN-2 and its closely related species, ARMAN-1. The enzyme consists of two duplicated catalytic units and one structural unit encoded on a single gene, representing a novel three-unit architecture. Homodimeric formation was confirmed by crosslinking assay, and site-directed mutagenesis determined that the conserved L10-pocket interaction between catalytic and structural unit is necessary for the assembly. A tRNA splicing assay reveal that ε2 endonuclease cleaves both canonical and noncanonical bulge–helix–bulge motifs, similar to that of (αβ)2 endonuclease. Unlike other ARMAN and Euryarchaeota, tRNAs found in ARMAN-2 are highly disrupted by introns at various positions, which again resemble the properties of archaeal species with (αβ)2 endonuclease. Thus, the discovery of ε2 endonuclease in an archaeon deeply branched within Euryarchaeota represents a new example of the coevolution of tRNA and their processing enzymes.
Research Organization:
University of California, Oakland, CA (United States)
Sponsoring Organization:
Institute for Fermentation; Ministry of Education, Culture, Sports, Science and Technology of Japan; Tsuruoka City Japan; USDOE Office of Science (SC), Biological and Environmental Research (BER); Yamagata Prefectural Government
Grant/Contract Number:
SC0004665
OSTI ID:
1904531
Journal Information:
Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 22 Vol. 39; ISSN 0305-1048
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

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Cited By (7)

Identification of highly-disrupted tRNA genes in nuclear genome of the red alga, Cyanidioschyzon merolae 10D journal July 2013
Reconstitution of the human tRNA splicing endonuclease complex: insight into the regulation of pre-tRNA cleavage journal June 2020
Update on RefSeq microbial genomes resources journal December 2014
The RNA-splicing endonuclease from the euryarchaeaon Methanopyrus kandleri is a heterotetramer with constrained substrate specificity journal January 2018
Identified Hybrid tRNA Structure Genes in Archaeal Genome journal September 2019
Circularly permuted tRNA genes: their expression and implications for their physiological relevance and development journal April 2014
Recent Insights Into the Structure, Function, and Evolution of the RNA-Splicing Endonucleases journal February 2019

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