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Comprehensive analysis of the pre-ribosomal RNA maturation pathway in a methanoarchaeon exposes the conserved circularization and linearization mode in archaea.

ABSTRACT: The ribosomal RNA (rRNA) genes are generally organized as an operon and cotranscribed into a polycistronic precursor; therefore, processing and maturation of pre-rRNAs are essential for ribosome biogenesis. However, rRNA maturation pathways of archaea, particularly of methanoarchaea, are scarcely known. Here, we thoroughly elucidated the maturation pathway of the rRNA operon (16S-tRNA^Ala-23S-tRNA^Cys-5S) in Methanolobus psychrophilus, one representative of methanoarchaea. Enzymatic assay demonstrated that EndA, a tRNA splicing endoribonuclease, cleaved bulge-helix-bulge (BHB) motifs buried in the processing stems of pre-16S and pre-23S rRNAs. Northern blot and quantitative PCR detected splicing-coupled circularization of pre-16S and pre-23S rRNAs, which accounted for 2% and 12% of the corresponding rRNAs, respectively. Importantly, endoribonuclease Nob1 was determined to linearize circular pre-16S rRNA at the mature 3' end so to expose the anti-Shine-Dalgarno sequence, while circular pre-23S rRNA was linearized at the mature 5' end by an unknown endoribonuclease. The resultant 5' and 3' extension in linearized pre-16S and pre-23S rRNAs were finally matured through 5'-3' and 3'-5' exoribonucleolytic trimming, respectively. Additionally, a novel processing pathway of endoribonucleolysis coupled with exoribonucleolysis was identified for the pre-5S rRNA maturation in this methanogen, which could be also conserved in most methanogenic euryarchaea. Based on evaluating the phylogenetic conservation of the key elements that are involved in circularization and linearization of pre-rRNA maturation, we predict that the rRNA maturation mode revealed here could be prevalent among archaea.

SUBMITTER: Qi L

PROVIDER: S-EPMC7549664 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:It has been proposed that the superphylum of Asgard Archaea may represent a historical link between the Archaea and Eukarya. Following the discovery of the Archaea, it was soon appreciated that archaeal ribosomes were more similar to those of Eukarya rather than Bacteria. Coupled with other eukaryotic-like features, it has been suggested that the Asgard Archaea may be directly linked to eukaryotes. However, the genomes of Bacteria and non-Asgard Archaea generally organize ribosome-related genes into clusters that likely function as operons. In contrast, eukaryotes typically do not employ an operon strategy. To gain further insight into conservation of the r-protein genes, the genome order of conserved ribosomal protein (r-protein) coding genes was identified in 17 Asgard genomes (thirteen complete genomes and four genomes with less than 20 contigs) and compared with those found previously in non-Asgard archaeal and bacterial genomes. A universal core of two clusters of 14 and 4 cooccurring r-proteins, respectively, was identified in both the Asgard and non-Asgard Archaea. The equivalent genes in the E. coli version of the cluster are found in the S10 and spc operons. The large cluster of 14 r-protein genes (uS19-uL22-uS3-uL29-uS17 from the S10 operon and uL14-uL24-uL5-uS14-uS8-uL6-uL18-uS5-uL30-uL15 from the spc operon) occurs as a complete set in the genomes of thirteen Asgard genomes (five Lokiarchaeotes, three Heimdallarchaeotes, one Odinarchaeote, and four Thorarchaeotes). Four less conserved clusters with partial bacterial equivalents were found in the Asgard. These were the L30e (str operon in Bacteria) cluster, the L18e (alpha operon in Bacteria) cluster, the S24e-S27ae-rpoE1 cluster, and the L31e, L12..L1 cluster. Finally, a new cluster referred to as L7ae was identified. In many cases, r-protein gene clusters/operons are less conserved in their organization in the Asgard group than in other Archaea. If this is generally true for nonribosomal gene clusters, the results may have implications for the history of genome organization. In particular, there may have been an early transition to or from the operon approach to genome organization. Other nonribosomal cellular features may support different relationships. For this reason, it may be important to consider ribosome features separately.

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Comprehensive analysis of the pre-ribosomal RNA maturation pathway in a methanoarchaeon exposes the conserved circularization and linearization mode in archaea.

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