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Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes.

Weinberg Z, Wang JX, Bogue J, Yang J, Corbino K, Moy RH, Breaker RR - Genome Biol. (2010)

Bottom Line: Structured RNAs can be detected by comparative genomics, in which homologous sequences are identified and inspected for mutations that conserve RNA secondary structure.Many noncoding RNAs that likely act in trans are also revealed, and several of the noncoding RNA candidates are found mostly or exclusively in metagenome DNA sequences.Given the sustained rate of RNA discovery over several similar projects, we expect that far more structured RNAs remain to be discovered from bacterial and archaeal organisms.

View Article: PubMed Central - HTML - PubMed

Affiliation: Howard Hughes Medical Institute, Yale University, New Haven, CT 06520-8103, USA. zasha.weinberg@yale.edu

ABSTRACT

Background: Structured noncoding RNAs perform many functions that are essential for protein synthesis, RNA processing, and gene regulation. Structured RNAs can be detected by comparative genomics, in which homologous sequences are identified and inspected for mutations that conserve RNA secondary structure.

Results: By applying a comparative genomics-based approach to genome and metagenome sequences from bacteria and archaea, we identified 104 candidate structured RNAs and inferred putative functions for many of these. Twelve candidate metabolite-binding RNAs were identified, three of which were validated, including one reported herein that binds the coenzyme S-adenosylmethionine. Newly identified cis-regulatory RNAs are implicated in photosynthesis or nitrogen regulation in cyanobacteria, purine and one-carbon metabolism, stomach infection by Helicobacter, and many other physiological processes. A candidate riboswitch termed crcB is represented in both bacteria and archaea. Another RNA motif may control gene expression from 3'-untranslated regions of mRNAs, which is unusual for bacteria. Many noncoding RNAs that likely act in trans are also revealed, and several of the noncoding RNA candidates are found mostly or exclusively in metagenome DNA sequences.

Conclusions: This work greatly expands the variety of highly structured noncoding RNAs known to exist in bacteria and archaea and provides a starting point for biochemical and genetic studies needed to validate their biologic functions. Given the sustained rate of RNA discovery over several similar projects, we expect that far more structured RNAs remain to be discovered from bacterial and archaeal organisms.

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Riboswitch candidates crcB, yjdF, wcaG, manA, pfl, epsC, and ykkC-III. Annotations are as described in Figure 1a. The transcription terminators that often overlap crcB or pfl RNAs are not depicted because they are not consistent in all representatives. They are annotated in Additional File 3. Question marks signify base-paired regions ("P4?" in yjdF, "P2?" in pfl, and "pseudoknot?" in manA) with weaker covariation or structural conservation. The pseudoknot in the epsC motif was predicted by others (Wade Winkler, personal communication, 2009). A portion of this figure was adapted from the supplementary data of a previous publication [21].
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Figure 2: Riboswitch candidates crcB, yjdF, wcaG, manA, pfl, epsC, and ykkC-III. Annotations are as described in Figure 1a. The transcription terminators that often overlap crcB or pfl RNAs are not depicted because they are not consistent in all representatives. They are annotated in Additional File 3. Question marks signify base-paired regions ("P4?" in yjdF, "P2?" in pfl, and "pseudoknot?" in manA) with weaker covariation or structural conservation. The pseudoknot in the epsC motif was predicted by others (Wade Winkler, personal communication, 2009). A portion of this figure was adapted from the supplementary data of a previous publication [21].

Mentions: The crcB motif (Figure 2) is detected in a wide variety of phyla in bacteria and archaea. Thus, crcB RNAs join only one known riboswitch class (TPP) [29], and few other classes of RNAs, that are present in more than one domain of life. The crcB motif consistently resides in the potential 5' UTRs of genes, including those involved in DNA repair (mutS), K+, or Cl- transport, or genes encoding formate hydrogen lyase. In many cases, predicted transcription terminators overlap the conserved crcB motif. Therefore, if ligand binding of the putative riboswitch stabilizes the conserved structure predicted for these RNAs, higher ligand concentrations are expected to inhibit terminator stem formation and increase gene expression.


Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes.

Weinberg Z, Wang JX, Bogue J, Yang J, Corbino K, Moy RH, Breaker RR - Genome Biol. (2010)

Riboswitch candidates crcB, yjdF, wcaG, manA, pfl, epsC, and ykkC-III. Annotations are as described in Figure 1a. The transcription terminators that often overlap crcB or pfl RNAs are not depicted because they are not consistent in all representatives. They are annotated in Additional File 3. Question marks signify base-paired regions ("P4?" in yjdF, "P2?" in pfl, and "pseudoknot?" in manA) with weaker covariation or structural conservation. The pseudoknot in the epsC motif was predicted by others (Wade Winkler, personal communication, 2009). A portion of this figure was adapted from the supplementary data of a previous publication [21].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2864571&req=5

Figure 2: Riboswitch candidates crcB, yjdF, wcaG, manA, pfl, epsC, and ykkC-III. Annotations are as described in Figure 1a. The transcription terminators that often overlap crcB or pfl RNAs are not depicted because they are not consistent in all representatives. They are annotated in Additional File 3. Question marks signify base-paired regions ("P4?" in yjdF, "P2?" in pfl, and "pseudoknot?" in manA) with weaker covariation or structural conservation. The pseudoknot in the epsC motif was predicted by others (Wade Winkler, personal communication, 2009). A portion of this figure was adapted from the supplementary data of a previous publication [21].
Mentions: The crcB motif (Figure 2) is detected in a wide variety of phyla in bacteria and archaea. Thus, crcB RNAs join only one known riboswitch class (TPP) [29], and few other classes of RNAs, that are present in more than one domain of life. The crcB motif consistently resides in the potential 5' UTRs of genes, including those involved in DNA repair (mutS), K+, or Cl- transport, or genes encoding formate hydrogen lyase. In many cases, predicted transcription terminators overlap the conserved crcB motif. Therefore, if ligand binding of the putative riboswitch stabilizes the conserved structure predicted for these RNAs, higher ligand concentrations are expected to inhibit terminator stem formation and increase gene expression.

Bottom Line: Structured RNAs can be detected by comparative genomics, in which homologous sequences are identified and inspected for mutations that conserve RNA secondary structure.Many noncoding RNAs that likely act in trans are also revealed, and several of the noncoding RNA candidates are found mostly or exclusively in metagenome DNA sequences.Given the sustained rate of RNA discovery over several similar projects, we expect that far more structured RNAs remain to be discovered from bacterial and archaeal organisms.

View Article: PubMed Central - HTML - PubMed

Affiliation: Howard Hughes Medical Institute, Yale University, New Haven, CT 06520-8103, USA. zasha.weinberg@yale.edu

ABSTRACT

Background: Structured noncoding RNAs perform many functions that are essential for protein synthesis, RNA processing, and gene regulation. Structured RNAs can be detected by comparative genomics, in which homologous sequences are identified and inspected for mutations that conserve RNA secondary structure.

Results: By applying a comparative genomics-based approach to genome and metagenome sequences from bacteria and archaea, we identified 104 candidate structured RNAs and inferred putative functions for many of these. Twelve candidate metabolite-binding RNAs were identified, three of which were validated, including one reported herein that binds the coenzyme S-adenosylmethionine. Newly identified cis-regulatory RNAs are implicated in photosynthesis or nitrogen regulation in cyanobacteria, purine and one-carbon metabolism, stomach infection by Helicobacter, and many other physiological processes. A candidate riboswitch termed crcB is represented in both bacteria and archaea. Another RNA motif may control gene expression from 3'-untranslated regions of mRNAs, which is unusual for bacteria. Many noncoding RNAs that likely act in trans are also revealed, and several of the noncoding RNA candidates are found mostly or exclusively in metagenome DNA sequences.

Conclusions: This work greatly expands the variety of highly structured noncoding RNAs known to exist in bacteria and archaea and provides a starting point for biochemical and genetic studies needed to validate their biologic functions. Given the sustained rate of RNA discovery over several similar projects, we expect that far more structured RNAs remain to be discovered from bacterial and archaeal organisms.

Show MeSH
Related in: MedlinePlus