mRNA-specific translation regulation by a ribosome-associated ncRNA in Haloferax volcanii

Wyss, Leander; Waser, Marco; Gebetsberger, Jennifer; Żywicki, Marek; Polacek, Norbert

doi:10.1038/s41598-018-30332-w

Cited by 25 publications

(20 citation statements)

References 37 publications

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“…Finally, a candidate itsRNA from the Halobacteria had several predicted targets associated with ribosomal proteins and proteins involved in translation processes. This finding, together with those from a recent study in H. volcanii (35), supports the idea of sRNA modulation of protein biosynthesis in the Archaea. A potential framework for mechanisms for sRNA regulation of translation might be provided by a report on the modular translation subsystems in the haloarchaeon Halobacterium salinarum that might selectively translate a subset of the transcriptome under specific growth conditions (36).…”

Section: Discussionsupporting

confidence: 87%

Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community

et al. 2020

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Regulatory small RNAs (sRNAs) play large-scale and essential roles in many cellular processes across all domains of life. Microbial sRNAs have been extensively studied in model organisms, but very little is known about the dynamics of sRNA synthesis and their roles in the natural environment. In this study, we discovered hundreds of intergenic (itsRNAs) and antisense (asRNAs) sRNAs expressed in an extremophilic microbial community inhabiting halite nodules (salt rocks) in the Atacama Desert. For this, we built SnapT, a new sRNA annotation pipeline that can be applied to any microbial community. We found asRNAs with expression levels negatively correlated with that of their overlapping putative target and itsRNAs that were conserved and significantly differentially expressed between 2 sampling time points. We demonstrated that we could perform target prediction and correlate expression levels between sRNAs and predicted target mRNAs at the community level. Functions of putative mRNA targets reflected the environmental challenges members of the halite communities were subjected to, including osmotic adjustments to a major rain event and competition for nutrients. IMPORTANCE Microorganisms in the natural world are found in communities, communicating and interacting with each other; therefore, it is essential that microbial regulatory mechanisms, such as gene regulation affected by small RNAs (sRNAs), be investigated at the community level. This work demonstrates that metatranscriptomic field experiments can link environmental variation with changes in RNA pools and have the potential to provide new insights into environmental sensing and responses in natural microbial communities through noncoding RNA-mediated gene regulation.

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Section: Discussionsupporting

confidence: 87%

Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community

et al. 2020

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“…By looking at asRNA loci covered by at least 20 reads along at least half its extension, we identified 91 asRNAs (~11%) with relevant signal (Table S12). Recently published rancRNA data in H. volcanii found 68 candidates antisense to genes, ~6% of their total [82].…”

Section: Resultsmentioning

confidence: 99%

The Primary Antisense Transcriptome of Halobacterium salinarum NRC-1

Almeida

Vêncio

Lorenzetti

et al. 2019

Genes

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Antisense RNAs (asRNAs) are present in diverse organisms and play important roles in gene regulation. In this work, we mapped the primary antisense transcriptome in the halophilic archaeon Halobacterium salinarum NRC-1. By reanalyzing publicly available data, we mapped antisense transcription start sites (aTSSs) and inferred the probable 3′ ends of these transcripts. We analyzed the resulting asRNAs according to the size, location, function of genes on the opposite strand, expression levels and conservation. We show that at least 21% of the genes contain asRNAs in H. salinarum. Most of these asRNAs are expressed at low levels. They are located antisense to genes related to distinctive characteristics of H. salinarum, such as bacteriorhodopsin, gas vesicles, transposases and other important biological processes such as translation. We provide evidence to support asRNAs in type II toxin–antitoxin systems in archaea. We also analyzed public Ribosome profiling (Ribo-seq) data and found that ~10% of the asRNAs are ribosome-associated non-coding RNAs (rancRNAs), with asRNAs from transposases overrepresented. Using a comparative transcriptomics approach, we found that ~19% of the asRNAs annotated in H. salinarum belong to genes with an ortholog in Haloferax volcanii, in which an aTSS could be identified with positional equivalence. This shows that most asRNAs are not conserved between these halophilic archaea.

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“…2A). An unrelated short archaeal ncRNA was used as binding specificity control [20] which resulted in no or very diminished binding to mammalian ribosomes. The obtained binding data with the tRNA Pro half are compatible with a binding site at or near the subunit interface.…”

Section: Expression and Ribosome-association Of The Trna Pro Half In mentioning

confidence: 99%

“…As negative binding control an archaeal ncRNA was used (5ʹ-CAGAGUAACCCCUCGGACGCAUCC ACAUGACCGAACUCAUCCCCCCUUCCCCCCUUCCCCA-UUAGGUUCGGUCACCCCUUUA-3) (ref. 20).…”

Section: Ribosome Filter Bindingmentioning

confidence: 99%

Modulation of mammalian translation by a ribosome-associated tRNA half

et al. 2020

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Originally considered futile degradation products, tRNA-derived RNA fragments (tdRs) have been shown over the recent past to be crucial players in orchestrating various cellular functions. Unlike other small non-coding RNA (ncRNA) classes, tdRs possess a multifaceted functional repertoire ranging from regulating transcription, apoptosis, RNA interference, ribosome biogenesis to controlling translation efficiency. A subset of the latter tdRs has been shown to directly target the ribosome, the central molecular machine of protein biosynthesis. Here we describe the function of the mammalian tRNA Pro 5ʹ half, a 35 residue long ncRNA associated with ribosomes and polysomes in several mammalian cell lines. Addition of tRNA Pro halves to mammalian in vitro translation systems results in global translation inhibition and concomitantly causes the upregulation of a specific low molecular weight translational product. This tRNA Pro 5ʹ half-dependent translation product consists of both RNA and amino acids. Transfection of the tRNA Pro half into HeLa cells leads to the formation of the same product in vivo. The migration of this product in acidic gels, the insensitivity to copper sulphate treatment, the resistance to 3ʹ polyadenylation, and the association with 80S monosomes indicate that the accumulated product is peptidyl-tRNA. Our data thus suggest that binding of the tRNA Pro 5ʹ half to the ribosome leads to ribosome stalling and to the formation of peptidyl-tRNA. Our findings revealed a so far unknown functional role of a tdR thus further enlarging the functional heterogeneity of this emerging class of ribo-regulators.

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mRNA-specific translation regulation by a ribosome-associated ncRNA in Haloferax volcanii

Cited by 25 publications

References 37 publications

Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community

Regulatory Noncoding Small RNAs Are Diverse and Abundant in an Extremophilic Microbial Community

The Primary Antisense Transcriptome of Halobacterium salinarum NRC-1

Modulation of mammalian translation by a ribosome-associated tRNA half

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