Physiological roles of small RNA molecules

Michaux, Charlotte; Verneuil, Nicolas; Hartke, Axel; Giard, Jean‐Christophe

doi:10.1099/mic.0.076208-0

Cited by 116 publications

(88 citation statements)

References 148 publications

(171 reference statements)

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“…Among these activities, we identified ethanolamine catabolism, amino acid metabolism, the regulation of carbohydrate metabolism, SRP-dependent cotranslational protein targeting to the membrane, gene silencing, and regulation of plasmid copy number as being represented in both sets (up-and downregulated) of DE sRNAs. A wide variety of studies have revealed that sRNAs are implicated in carbon metabolism, transport, and amino acid metabolism (45), protein transport by SRP-dependent cotranslational protein targeting (57), and control of plasmid copy number (58,59). Some of these processes have been linked to bacterial pathogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…This is especially true in the oral cavity, where conditions change daily in short periods of time due to the ingestion of nutrients and to the fact that the oral cavity is an open entrance in contact with the external environment, hence the importance of regulatory elements such as sRNAs, which are rapidly synthesized and capable of modulating the metabolism faster than regulation involving protein synthesis (43,44). It is now well established that sRNAs are capable of performing a wide variety of physiological roles, including adapting to new environmental conditions through quorum-sensing systems or the development of biofilms (45). Recent reports have shown that sRNAs also play important roles in microbial virulence and infection (46,47).…”

Section: Discussionmentioning

confidence: 99%

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Small RNA Transcriptome of the Oral Microbiome during Periodontitis Progression

Duran-Pinedo¹,

Yost²,

Frias-Lopez

2015

Appl Environ Microbiol

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The oral microbiome is one of the most complex microbial communities in the human body, and due to circumstances not completely understood, the healthy microbial community becomes dysbiotic, giving rise to periodontitis, a polymicrobial inflammatory disease. We previously reported the results of community-wide gene expression changes in the oral microbiome during periodontitis progression and identified signatures associated with increasing severity of the disease. Small noncoding RNAs (sRNAs) are key players in posttranscriptional regulation, especially in fast-changing environments such as the oral cavity. Here, we expanded our analysis to the study of the sRNA metatranscriptome during periodontitis progression on the same samples for which mRNA expression changes were analyzed. We observed differential expression of 12,097 sRNAs, identifying a total of 20 Rfam sRNA families as being overrepresented in progression and 23 at baseline. Gene ontology activities regulated by the differentially expressed (DE) sRNAs included amino acid metabolism, ethanolamine catabolism, signal recognition particle-dependent cotranslational protein targeting to membrane, intron splicing, carbohydrate metabolism, control of plasmid copy number, and response to stress. In integrating patterns of expression of protein coding transcripts and sRNAs, we found that functional activities of genes that correlated positively with profiles of expression of DE sRNAs were involved in pathogenesis, proteolysis, ferrous iron transport, and oligopeptide transport. These findings represent the first integrated sequencing analysis of the community-wide sRNA transcriptome of the oral microbiome during periodontitis progression and show that sRNAs are key regulatory elements of the dysbiotic process leading to disease. Bacterial small noncoding RNAs (sRNAs) encompass a large and diverse group of RNA molecules that do not result in the translation of a protein product. They show high heterogeneity in size and structure and many are used in regulatory roles or other functional capacities upon transcription. sRNAs are important in bacteria because they can be used to adapt rapidly to changing environmental conditions, especially in an environment such as the oral cavity, which is exposed daily to regular changes in amount and quality of nutrients available for use by the oral biofilms. Most of these sRNAs are encoded in the 5= and 3= untranslated regions, as well as in intergenic regions (IGRs) of the genome (1).sRNAs display a wide variety of mechanisms of action. sRNAs repress translation of mRNA by attaching to the ribosome binding site (RBS) competing with the ribosome and leading to the rapid degradation of the mRNA (2). Other noncanonical mechanisms of translation repression have been also described, such as binding cis-acting antisense RNA to a ribosome standby site upstream of the RBS (3). In addition, sRNAs can also activate the translations of mRNAs (4, 5) or can modulate gene expression by varying the level of transcript stability (6). sRNA ca...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Small RNA Transcriptome of the Oral Microbiome during Periodontitis Progression

Duran-Pinedo¹,

Yost²,

Frias-Lopez

2015

Appl Environ Microbiol

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“…Since sRNAs play versatile roles in the bacterial cell, a determined sRNA profile guarantees a quick and precise process of gene regulation and physiological adaptation to an ever-changing environment, which may be necessary for the establishment of a bacterial pathogenic lifestyle (Michaux et al 2014b).…”

Section: Introductionmentioning

confidence: 99%

“…Most sRNAs can be divided into the following four broad categories: (i) cis-acting RNAs; trans-acting RNAs that may either (ii) modulate protein activity or (iii) bind to mRNAs; and (iv) clustered regularly interspaced short palindromic repeats-CRISPRs (Michaux et al 2014b). The most studied bacterial sRNAs are the ones coded in trans, which exert their cellular roles by base pairing with mRNA targets to attenuate, stop, or activate their translation (Man et al 2011;Papenfort and Vanderpool 2015).…”

Section: Introductionmentioning

confidence: 99%

A computational strategy for the search of regulatory small RNAs in Actinobacillus pleuropneumoniae

Rossi

Bossé

et al. 2016

RNA

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Bacterial regulatory small RNAs (sRNAs) play important roles in gene regulation and are frequently connected to the expression of virulence factors in diverse bacteria. Only a few sRNAs have been described for Pasteurellaceae pathogens and no in-depth analysis of sRNAs has been described for Actinobacillus pleuropneumoniae, the causative agent of porcine pleuropneumonia, responsible for considerable losses in the swine industry. To search for sRNAs in A. pleuropneumoniae, we developed a strategy for the computational analysis of the bacterial genome by using four algorithms with different approaches, followed by experimental validation. The coding strand and expression of 17 out of 23 RNA candidates were confirmed by Northern blotting, RT-PCR, and RNA sequencing. Among them, two are likely riboswitches, three are housekeeping regulatory RNAs, two are the widely studied GcvB and 6S sRNAs, and 10 are putative novel trans-acting sRNAs, never before described for any bacteria. The latter group has several potential mRNA targets, many of which are involved with virulence, stress resistance, or metabolism, and connect the sRNAs in a complex gene regulatory network. The sRNAs identified are well conserved among the Pasteurellaceae that are evolutionarily closer to A. pleuropneumoniae and/or share the same host. Our results show that the combination of newly developed computational programs can be successfully utilized for the discovery of novel sRNAs and indicate an intricate system of gene regulation through sRNAs in A. pleuropneumoniae and in other Pasteurellaceae, thus providing clues for novel aspects of virulence that will be explored in further studies.

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“…These short functional RNAs greatly vary in structure and in mechanism of action. 23,24 To achieve genetic regulation, sRNAs often imperfectly base-pair with a set of given mRNAs, 25 resulting in various outcomes (repression of translation, mRNA degradation or translation enhancement). 23 A single sRNA can even adopt different mechanisms of action depending on the mRNA targeted.…”

mentioning

confidence: 99%