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Origin, Evolution, and Loss of Bacterial Small RNAs

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  • Authors: H. Auguste Dutcher1, Rahul Raghavan2
  • Editors: Gisela Storz3, Kai Papenfort4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biology and Center for Life in Extreme Environments, Portland State University, Portland, OR 97201; 2: Department of Biology and Center for Life in Extreme Environments, Portland State University, Portland, OR 97201; 3: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 4: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0004-2017
  • Received 29 October 2017 Accepted 24 January 2018 Published 06 April 2018
  • Rahul Raghavan, [email protected]
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  • Abstract:

    Despite the central role of bacterial noncoding small RNAs (sRNAs) in posttranscriptional regulation, little is understood about their evolution. Here we compile what has been studied to date and trace a life cycle of sRNAs—from their mechanisms of emergence, through processes of change and frequent neofunctionalization, to their loss from bacterial lineages. Because they possess relatively unrestrictive structural requirements, we find that sRNA origins are varied, and include emergence as well as formation from preexisting genetic elements via duplication events and horizontal gene transfer. The need for only partial complementarity to their mRNA targets facilitates apparent rapid change, which also contributes to significant challenges in tracing sRNAs across broad evolutionary distances. We document that recently emerged sRNAs in particular evolve quickly, mirroring dynamics observed in microRNAs, their functional analogs in eukaryotes. Mutations in mRNA-binding regions, transcriptional regulator or sigma factor binding sites, and protein-binding regions are all likely sources of shifting regulatory roles of sRNAs. Finally, using examples from the few evolutionary studies available, we examine cases of sRNA loss and describe how these may be the result of adaptive in addition to neutral processes. We highlight the need for more-comprehensive analyses of sRNA evolutionary patterns as a means to improve novel sRNA detection, enhance genome annotation, and deepen our understanding of regulatory networks in bacteria.

  • Citation: Dutcher H, Raghavan R. 2018. Origin, Evolution, and Loss of Bacterial Small RNAs. Microbiol Spectrum 6(2):RWR-0004-2017. doi:10.1128/microbiolspec.RWR-0004-2017.

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/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0004-2017
2018-04-06
2018-09-18

Abstract:

Despite the central role of bacterial noncoding small RNAs (sRNAs) in posttranscriptional regulation, little is understood about their evolution. Here we compile what has been studied to date and trace a life cycle of sRNAs—from their mechanisms of emergence, through processes of change and frequent neofunctionalization, to their loss from bacterial lineages. Because they possess relatively unrestrictive structural requirements, we find that sRNA origins are varied, and include emergence as well as formation from preexisting genetic elements via duplication events and horizontal gene transfer. The need for only partial complementarity to their mRNA targets facilitates apparent rapid change, which also contributes to significant challenges in tracing sRNAs across broad evolutionary distances. We document that recently emerged sRNAs in particular evolve quickly, mirroring dynamics observed in microRNAs, their functional analogs in eukaryotes. Mutations in mRNA-binding regions, transcriptional regulator or sigma factor binding sites, and protein-binding regions are all likely sources of shifting regulatory roles of sRNAs. Finally, using examples from the few evolutionary studies available, we examine cases of sRNA loss and describe how these may be the result of adaptive in addition to neutral processes. We highlight the need for more-comprehensive analyses of sRNA evolutionary patterns as a means to improve novel sRNA detection, enhance genome annotation, and deepen our understanding of regulatory networks in bacteria.

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Figures

Image of FIGURE 1
FIGURE 1

sRNA origin, functional divergence, and loss. (a) sRNA sources include duplication events, HGT, and origination via promoter emergence. (b) Sequence and structural changes are often accompanied by differential sRNA gene expression and accumulation of mRNA targets and/or protein-binding regions, causing the sRNA to become fully integrated into regulatory networks. (c) sRNA loss occurs through mutations that erode promoter sequences, genome rearrangements that split sRNA-containing IGRs, and selective pressures that prompt shifts in network interactions.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0004-2017
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Image of FIGURE 2
FIGURE 2

Sequence conservation and structure of an sRNA gene. (a) Sequence conservation within an sRNA gene (orange) and flanking protein-coding genes (blue). The black line represents nucleotide diversity index, π, calculated using a sliding-window analysis; the flanking green lines indicate the 95% confidence interval. Lowest nucleotide polymorphism within sRNA genes is observed in mRNA-binding regions. (b) Predicted structure of an sRNA, showing a single-stranded mRNA-binding site and a terminator hairpin. Adapted from reference 21 with permission.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0004-2017
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