Transcriptomic profiling of the oyster pathogen <i>Vibrio splendidus</i> opens a window on the evolutionary dynamics of the small RNA repertoire in the <i>Vibrio</i> genus

Toffano‐Nioche, Claire; Nguyen, Aithanh; Kuchly, Claire; Ott, Alban; Gautheret, Daniel; Bouloc, Philippe; Jacq, Annick

doi:10.1261/rna.033324.112

Cited by 41 publications

(53 citation statements)

References 83 publications

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“…Given the lack of general antisense RNA conservation found both within the streptomycetes in this study, and in other bacteria [49], we were surprised to identify a strongly-expressed cis -antisense RNA within a hopanoid biosynthetic cluster in S. coelicolor and S. avermitilis (Figure 5A). Hopanoids are cholesterol-like pentacyclic molecules [50-52] found throughout bacteria [53].…”

Section: Resultsmentioning

confidence: 67%

Comparative analysis of non-coding RNAs in the antibiotic-producing Streptomyces bacteria

et al. 2013

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BackgroundNon-coding RNAs (ncRNAs) are key regulatory elements that control a wide range of cellular processes in all bacteria in which they have been studied. Taking advantage of recent technological innovations, we set out to fully explore the ncRNA potential of the multicellular, antibiotic-producing Streptomyces bacteria.ResultsUsing a comparative RNA sequencing analysis of three divergent model streptomycetes (S. coelicolor, S. avermitilis and S. venezuelae), we discovered hundreds of novel cis-antisense RNAs and intergenic small RNAs (sRNAs). We identified a ubiquitous antisense RNA species that arose from the overlapping transcription of convergently-oriented genes; we termed these RNA species ‘cutoRNAs’, for convergent untranslated overlapping RNAs. Conservation between different classes of ncRNAs varied greatly, with sRNAs being more conserved than antisense RNAs. Many species-specific ncRNAs, including many distinct cutoRNA pairs, were located within antibiotic biosynthetic clusters, including the actinorhodin, undecylprodigiosin, and coelimycin clusters of S. coelicolor, the chloramphenicol cluster of S. venezuelae, and the avermectin cluster of S. avermitilis.ConclusionsThese findings indicate that ncRNAs, including a novel class of antisense RNA, may exert a previously unrecognized level of regulatory control over antibiotic production in these bacteria. Collectively, this work has dramatically expanded the ncRNA repertoire of three Streptomyces species and has established a critical foundation from which to investigate ncRNA function in this medically and industrially important bacterial genus.

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Section: Resultsmentioning

confidence: 67%

Comparative analysis of non-coding RNAs in the antibiotic-producing Streptomyces bacteria

et al. 2013

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“…It should be noted that lack of conservation of specific promoters does not necessarily indicate a lack of functional importance, but could instead reflect lineage‐specific evolution. Indeed, regulatory small RNAs are often poorly conserved, even between closely related species (Toffano‐Nioche et al ., ; Beauregard et al ., ; Patenge et al ., ). However, our analysis of conservation within E. coli suggests that most intragenic FliA promoters are not conserved even within the species, although this multi‐promoter analysis does not rule out the possibility that a small proportion of the intragenic promoters are functional.…”

Section: Discussionmentioning

confidence: 98%

The evolutionary impact of intragenic FliA promoters in proteobacteria

Fitzgerald

Smith

Lapierre

et al. 2018

Molecular Microbiology

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In Escherichia coli, one sigma factor recognizes the majority of promoters, and six 'alternative' sigma factors recognize specific subsets of promoters. The alternative sigma factor FliA (σ ) recognizes promoters upstream of many flagellar genes. We previously showed that most E. coli FliA binding sites are located inside genes. However, it was unclear whether these intragenic binding sites represent active promoters. Here, we construct and assay transcriptional promoter-lacZ fusions for all 52 putative FliA promoters previously identified by ChIP-seq. These experiments, coupled with integrative analysis of published genome-scale transcriptional datasets, strongly suggest that most intragenic FliA binding sites are active promoters that transcribe highly unstable RNAs. Additionally, we show that widespread intragenic FliA-dependent transcription may be a conserved phenomenon, but that specific promoters are not themselves conserved. We conclude that intragenic FliA-dependent promoters and the resulting RNAs are unlikely to have important regulatory functions. Nonetheless, one intragenic FliA promoter is broadly conserved and constrains evolution of the overlapping protein-coding gene. Thus, our data indicate that intragenic regulatory elements can influence bacterial protein evolution and suggest that the impact of intragenic regulatory sequences on genome evolution should be considered more broadly.

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“…It should be noted that lack of conservation of specific promoters does not necessarily indicate a lack of functional importance, but could instead reflect lineage-specific evolution. Indeed, regulatory small RNAs are often poorly conserved, even between closely related species [32-34]. Consistent with this, one of the two stable, FliA-transcribed non-coding RNAs - that transcribed from within uhpT - is likely a functional regulator, despite a lack of promoter conservation.…”

Section: Discussionmentioning

confidence: 99%

The evolutionary impact of Intragenic FliA Promoters in Proteobacteria

Fitzgerald

Smith

Lapierre

et al. 2017

Preprint

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21Recent work has revealed that large numbers of promoters in bacteria are located inside genes. In contrast, almost all studies 22 of transcription have focused on promoters upstream of genes. Bacterial promoters are recognized by Sigma factors that 23 associate with initiating RNA polymerase. In Escherichia coli, one Sigma factor recognizes the majority of promoters, and 24 six "alternative" Sigma factors recognize specific subsets of promoters. One of these alternative Sigma factors, FliA (σ 28 ), Nonetheless, one intragenic FliA promoter is highly conserved, and we show that this promoter constrains 50 evolution of the overlapping protein-coding gene. Given the enormous number of regulatory DNA sites within 51 genes, we propose that the evolution of many genes is constrained by these elements.

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Transcriptomic profiling of the oyster pathogen Vibrio splendidus opens a window on the evolutionary dynamics of the small RNA repertoire in the Vibrio genus

Cited by 41 publications

References 83 publications

Comparative analysis of non-coding RNAs in the antibiotic-producing Streptomyces bacteria

Comparative analysis of non-coding RNAs in the antibiotic-producing Streptomyces bacteria

The evolutionary impact of intragenic FliA promoters in proteobacteria

The evolutionary impact of Intragenic FliA Promoters in Proteobacteria

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