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Chapter 28 : Origin, Evolution, and Loss of Bacterial Small RNAs

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Origin, Evolution, and Loss of Bacterial Small RNAs, Page 1 of 2

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Abstract:

As our understanding of the transcriptional landscape of bacteria continues to expand, it has become clear that noncoding small RNAs (sRNAs) play a pivotal regulatory role ( ). Typically 50 to 400 nucleotides in length, sRNAs posttranscriptionally regulate gene expression, usually by base-pairing with one or more mRNA targets ( ). sRNAs likely provide certain advantages over protein regulators because they act quickly, are relatively metabolically inexpensive, and provide an additional way to respond to environmental signals ( ). Beyond these basic characteristics, however, the roles of bacterial sRNAs are extremely diverse: they are capable of upregulating or downregulating translation, stabilizing mRNAs or targeting them for degradation, sharing targets, and/or targeting multiple mRNAs. Variability in their sequence, structure, and how and when they are transcribed allows them to meet a wide range of nuanced regulatory needs based on the diverse environments to which bacteria must adapt.

Citation: Dutcher H, Raghavan R. 2019. Origin, Evolution, and Loss of Bacterial Small RNAs, p 487-497. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0004-2017
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Figures

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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.

Citation: Dutcher H, Raghavan R. 2019. Origin, Evolution, and Loss of Bacterial Small RNAs, p 487-497. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. 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 with permission.

Citation: Dutcher H, Raghavan R. 2019. Origin, Evolution, and Loss of Bacterial Small RNAs, p 487-497. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0004-2017
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References

/content/book/10.1128/9781683670247.chap28
1. Beisel CL,, Storz G . 2010. Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34 : 866 882.[PubMed]
2. Gottesman S,, Storz G . 2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3 : a003798.[CrossRef][PubMed]
3. Nitzan M,, Rehani R,, Margalit H . 2017. Integration of bacterial small RNAs in regulatory networks. Annu Rev Biophys 46 : 131 148.[PubMed]
4. Storz G,, Vogel J,, Wassarman KM . 2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43 : 880 891.[PubMed]
5. Updegrove TB,, Shabalina SA,, Storz G . 2015. How do base-pairing small RNAs evolve? FEMS Microbiol Rev 39 : 379 391.[PubMed]
6. Hoeppner MP,, Gardner PP,, Poole AM . 2012. Comparative analysis of RNA families reveals distinct repertoires for each domain of life. PLoS Comput Biol 8 : e1002752.[CrossRef][PubMed]
7. Nawrocki EP,, Burge SW,, Bateman A,, Daub J,, Eberhardt RY,, Eddy SR,, Floden EW,, Gardner PP,, Jones TA,, Tate J,, Finn RD . 2015. Rfam 12.0: updates to the RNA families database. Nucleic Acids Res 43( Database issue) : D130 D137.[PubMed]
8. Finn RD,, Coggill P,, Eberhardt RY,, Eddy SR,, Mistry J,, Mitchell AL,, Potter SC,, Punta M,, Qureshi M,, Sangrador-Vegas A,, Salazar GA,, Tate J,, Bateman A . 2016. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44( D1) : D279 D285.[PubMed]
9. Lindgreen S,, Umu SU,, Lai AS,, Eldai H,, Liu W,, McGimpsey S,, Wheeler NE,, Biggs PJ,, Thomson NR,, Barquist L,, Poole AM,, Gardner PP . 2014. Robust identification of noncoding RNA from transcriptomes requires phylogenetically-informed sampling. PLoS Comput Biol 10 : e1003907.[CrossRef][PubMed]
10. Huerta AM,, Francino MP,, Morett E,, Collado-Vides J . 2006. Selection for unequal densities of σ 70 promoter-like signals in different regions of large bacterial genomes. PLoS Genet 2 : e185.[CrossRef][PubMed]
11. Rivas E,, Eddy SR . 2000. Secondary structure alone is generally not statistically significant for the detection of noncoding RNAs. Bioinformatics 16 : 583 605.[PubMed]
12. Zhang Y,, Huang H,, Zhang D,, Qiu J,, Yang J,, Wang K,, Zhu L,, Fan J,, Yang J . 2017. A review on recent computational methods for predicting noncoding RNAs. BioMed Res Int 2017 : 9139504.[CrossRef][PubMed]
13. Gardner PP,, Wilm A,, Washietl S . 2005. A benchmark of multiple sequence alignment programs upon structural RNAs. Nucleic Acids Res 33 : 2433 2439.[PubMed]
14. Zhang J . 2003. Evolution by gene duplication: an update. Trends Ecol Evol 18 : 292 298.
15. Ochman H,, Lawrence JG,, Groisman EA . 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405 : 299 304.[PubMed]
16. Schlötterer C . 2015. Genes from scratch—the evolutionary fate of de novo genes. Trends Genet 31 : 215 219.[PubMed]
17. Tautz D,, Domazet-Lošo T . 2011. The evolutionary origin of orphan genes. Nat Rev Genet 12 : 692 702.[PubMed]
18. Lyu Y,, Shen Y,, Li H,, Chen Y,, Guo L,, Zhao Y,, Hungate E,, Shi S,, Wu CI,, Tang T . 2014. New microRNAs in Drosophila—birth, death and cycles of adaptive evolution. PLoS Genet 10 : e1004096.[CrossRef][PubMed]
19. Peer A,, Margalit H . 2011. Accessibility and evolutionary conservation mark bacterial small-RNA target-binding regions. J Bacteriol 193 : 1690 1701.[PubMed]
20. Richter AS,, Backofen R . 2012. Accessibility and conservation: general features of bacterial small RNA-mRNA interactions? RNA Biol 9 : 954 965.[PubMed]
21. Kacharia FR,, Millar JA,, Raghavan R . 2017. Emergence of new sRNAs in enteric bacteria is associated with low expression and rapid evolution. J Mol Evol 84 : 204 213.[PubMed]
22. Kaessmann H . 2010. Origins, evolution, and phenotypic impact of new genes. Genome Res 20 : 1313 1326.[PubMed]
23. Capra JA,, Pollard KS,, Singh M . 2010. Novel genes exhibit distinct patterns of function acquisition and network integration. Genome Biol 11 : R127.[PubMed]
24. Caswell CC,, Oglesby-Sherrouse AG,, Murphy ER . 2014. Sibling rivalry: related bacterial small RNAs and their redundant and non-redundant roles. Front Cell Infect Microbiol 4 : 151.[CrossRef][PubMed]
25. Wilderman PJ,, Sowa NA,, FitzGerald DJ,, FitzGerald PC,, Gottesman S,, Ochsner UA,, Vasil ML . 2004. Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc Natl Acad Sci U S A 101 : 9792 9797.[PubMed]
26. Padalon-Brauch G,, Hershberg R,, Elgrably-Weiss M,, Baruch K,, Rosenshine I,, Margalit H,, Altuvia S . 2008. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36 : 1913 1927.[PubMed]
27. Lenz DH,, Mok KC,, Lilley BN,, Kulkarni RV,, Wingreen NS,, Bassler BL,, Way I . 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118 : 69 82.[PubMed]
28. del Val C,, Rivas E,, Torres-Quesada O,, Toro N,, Jiménez-Zurdo JI . 2007. Identification of differentially expressed small non-coding RNAs in the legume endosymbiont Sinorhizobium meliloti by comparative genomics. Mol Microbiol 66 : 1080 1091.[PubMed]
29. Wilms I,, Voss B,, Hess WR,, Leichert LI,, Narberhaus F . 2011. Small RNA-mediated control of the Agrobacterium tumefaciens GABA binding protein. Mol Microbiol 80 : 492 506.[PubMed]
30. Torres-Quesada O,, Millán V,, Nisa-Martínez R,, Bardou F,, Crespi M,, Toro N,, Jiménez-Zurdo JI . 2013. Independent activity of the homologous small regulatory RNAs AbcR1 and AbcR2 in the legume symbiont Sinorhizobium meliloti. PLoS One 8 : e68147.[CrossRef][PubMed]
31. Papenfort K,, Vogel J . 2009. Multiple target regulation by small noncoding RNAs rewires gene expression at the post-transcriptional level. Res Microbiol 160 : 278 287.[PubMed]
32. Skippington E,, Ragan MA . 2012. Evolutionary dynamics of small RNAs in 27 Escherichia coli and Shigella genomes. Genome Biol Evol 4 : 330 345.[PubMed]
33. Brantl S,, Jahn N . 2015. sRNAs in bacterial type I and type III toxin-antitoxin systems. FEMS Microbiol Rev 39 : 413 427.[PubMed]
34. Chabelskaya S,, Gaillot O,, Felden B . 2010. A Staphylococcus aureus small RNA is required for bacterial virulence and regulates the expression of an immune-evasion molecule. PLoS Pathog 6 : e1000927.[CrossRef][PubMed]
35. Gong H,, Vu GP,, Bai Y,, Chan E,, Wu R,, Yang E,, Liu F,, Lu S . 2011. A Salmonella small non-coding RNA facilitates bacterial invasion and intracellular replication by modulating the expression of virulence factors. PLoS Pathog 7 : e1002120.[CrossRef][PubMed]
36. Lee YH,, Kim S,, Helmann JD,, Kim BH,, Park YK . 2013. RaoN, a small RNA encoded within Salmonella pathogenicity island-11, confers resistance to macrophage-induced stress. Microbiology 159 : 1366 1378.[PubMed]
37. Hershko-Shalev T,, Odenheimer-Bergman A,, Elgrably-Weiss M,, Ben-Zvi T,, Govindarajan S,, Seri H,, Papenfort K,, Vogel J,, Altuvia S . 2016. Gifsy-1 prophage IsrK with dual function as small and messenger RNA modulates vital bacterial machineries. PLoS Genet 12 : e1005975.[CrossRef][PubMed]
38. Sabath N,, Wagner A,, Karlin D . 2012. Evolution of viral proteins originated de novo by overprinting. Mol Biol Evol 29 : 3767 3780.[PubMed]
39. Piriyapongsa J,, Jordan IK . 2007. A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS One 2 : e203.[CrossRef][PubMed]
40. Chen Y,, Zhou F,, Li G,, Xu Y . 2008. A recently active miniature inverted-repeat transposable element, Chunjie, inserted into an operon without disturbing the operon structure in Geobacter uraniireducens Rf4. Genetics 179 : 2291 2297.[PubMed]
41. Raghavan R,, Kacharia FR,, Millar JA,, Sislak CD,, Ochman H . 2015. Genome rearrangements can make and break small RNA genes. Genome Biol Evol 7 : 557 566.[PubMed]
42. Heinen TJ,, Staubach F,, Häming D,, Tautz D . 2009. Emergence of a new gene from an intergenic region. Curr Biol 19 : 1527 1531.[PubMed]
43. Peterman N,, Lavi-Itzkovitz A,, Levine E . 2014. Large-scale mapping of sequence-function relations in small regulatory RNAs reveals plasticity and modularity. Nucleic Acids Res 42 : 12177 12188.[PubMed]
44. Piriyapongsa J,, Mariño-Ramírez L,, Jordan IK . 2007. Origin and evolution of human microRNAs from transposable elements. Genetics 176 : 1323 1337.[PubMed]
45. Smalheiser NR,, Torvik VI . 2005. Mammalian microRNAs derived from genomic repeats. Trends Genet 21 : 322 326.[PubMed]
46. Peer A,, Margalit H . 2014. Evolutionary patterns of Escherichia coli small RNAs and their regulatory interactions. RNA 20 : 994 1003.[PubMed]
47. Chen K,, Rajewsky N . 2007. The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 8 : 93 103.[PubMed]
48. Jovelin R,, Cutter AD . 2014. Microevolution of nematode miRNAs reveals diverse modes of selection. Genome Biol Evol 6 : 3049 3063.[PubMed]
49. Papenfort K,, Förstner KU,, Cong JP,, Sharma CM,, Bassler BL . 2015. Differential RNA-seq of Vibrio cholerae identifies the VqmR small RNA as a regulator of biofilm formation. Proc Natl Acad Sci U S A 112 : E766 E775.[PubMed]
50. Otoupal PB,, Erickson KE,, Escalas-Bordoy A,, Chatterjee A . 2017. CRISPR perturbation of gene expression alters bacterial fitness under stress and reveals underlying epistatic sonstraints. ACS Synth Biol 6 : 94 107.[PubMed]
51. Massé E,, Vanderpool CK,, Gottesman S . 2005. Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187 : 6962 6971.[PubMed]
52. Göpel Y,, Lüttmann D,, Heroven AK,, Reichenbach B,, Dersch P,, Görke B . 2011. Common and divergent features in transcriptional control of the homologous small RNAs GlmY and GlmZ in Enterobacteriaceae. Nucleic Acids Res 39 : 1294 1309.[PubMed]
53. Göpel Y,, Papenfort K,, Reichenbach B,, Vogel J,, Görke B . 2013. Targeted decay of a regulatory small RNA by an adaptor protein for RNase E and counteraction by an anti-adaptor RNA. Genes Dev 27 : 552 564.[PubMed]
54. Massé E,, Gottesman S . 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 99 : 4620 4625.[PubMed]
55. Udekwu KI,, Darfeuille F,, Vogel J,, Reimegård J,, Holmqvist E,, Wagner EG . 2005. Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 19 : 2355 2366.[PubMed]
56. Song T,, Mika F,, Lindmark B,, Liu Z,, Schild S,, Bishop A,, Zhu J,, Camilli A,, Johansson J,, Vogel J,, Wai SN . 2008. A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles. Mol Microbiol 70 : 100 111.[PubMed]
57. Chen IK,, Velicer GJ,, Yu YN . 2017. Divergence of functional effects among bacterial sRNA paralogs. BMC Evol Biol 17 : 199.[CrossRef][PubMed]
58. Azam MS,, Vanderpool CK . 2017. Translational regulation by bacterial small RNAs via an unusual Hfq-dependent mechanism. Nucleic Acids Res.[CrossRef]
59. Feng L,, Rutherford ST,, Papenfort K,, Bagert JD,, van Kessel JC,, Tirrell DA,, Wingreen NS,, Bassler BL . 2015. A Qrr noncoding RNA deploys four different regulatory mechanisms to optimize quorum-sensing dynamics. Cell 160 : 228 240.[PubMed]
60. Robinson KE,, Orans J,, Kovach AR,, Link TM,, Brennan RG . 2014. Mapping Hfq-RNA interaction surfaces using tryptophan fluorescence quenching. Nucleic Acids Res 42 : 2736 2749.[PubMed]
61. Smirnov A,, Förstner KU,, Holmqvist E,, Otto A,, Günster R,, Becher D,, Reinhardt R,, Vogel J . 2016. Grad-seq guides the discovery of ProQ as a major small RNA-binding protein. Proc Natl Acad Sci U S A 113 : 11591 11596.[PubMed]
62. Smirnov A,, Wang C,, Drewry LL,, Vogel J . 2017. Molecular mechanism of mRNA repression in trans by a ProQ-dependent small RNA. EMBO J 36 : 1029 1045.[PubMed]
63. Cerutti F,, Mallet L,, Painset A,, Hoede C,, Moisan A,, Bécavin C,, Duval M,, Dussurget O,, Cossart P,, Gaspin C,, Chiapello H . 2017. Unraveling the evolution and coevolution of small regulatory RNAs and coding genes in Listeria. BMC Genomics 18 : 882.[CrossRef][PubMed]
64. Ellis MJ,, Trussler RS,, Charles O,, Haniford DB . 2017. A transposon-derived small RNA regulates gene expression in Salmonella Typhimurium. Nucleic Acids Res 45 : 5470 5486.[PubMed]
65. Lybecker M,, Bilusic I,, Raghavan R . 2014. Pervasive transcription: detecting functional RNAs in bacteria. Transcription 5 : e944039.[CrossRef][PubMed]
66. Bilusic I,, Popitsch N,, Rescheneder P,, Schroeder R,, Lybecker M . 2014. Revisiting the coding potential of the E. coli genome through Hfq co-immunoprecipitation. RNA Biol 11 : 641 654.[PubMed]
67. Chao Y,, Papenfort K,, Reinhardt R,, Sharma CM,, Vogel J . 2012. An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31 : 4005 4019.[PubMed]
68. Rolland K,, Lambert-Zechovsky N,, Picard B,, Denamur E . 1998. Shigella and enteroinvasive Escherichia coli strains are derived from distinct ancestral strains of E. coli. Microbiology 144 : 2667 2672.
69. van den Beld MJ,, Reubsaet FA . 2012. Differentiation between Shigella, enteroinvasive Escherichia coli (EIEC) and noninvasive Escherichia coli. Eur J Clin Microbiol Infect Dis 31 : 899 904.[PubMed]
70. Lan R,, Alles MC,, Donohoe K,, Martinez MB,, Reeves PR,, Martinez MB . 2004. Molecular evolutionary relationships of enteroinvasive Escherichia coli and Shigella spp. Infect Immun 72 : 5080 5088.[PubMed]
71. Parsot C . 2005. Shigella spp. and enteroinvasive Escherichia coli pathogenicity factors. FEMS Microbiol Lett 252 : 11 18.[PubMed]
72. Day WA Jr,, Fernández RE,, Maurelli AT . 2001. Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect Immun 69 : 7471 7480.[PubMed]
73. Koskiniemi S,, Sun S,, Berg OG,, Andersson DI . 2012. Selection-driven gene loss in bacteria. PLoS Genet 8 : e1002787.[CrossRef][PubMed]
74. Hottes AK,, Freddolino PL,, Khare A,, Donnell ZN,, Liu JC,, Tavazoie S . 2013. Bacterial adaptation through loss of function. PLoS Genet 9 : e1003617.[CrossRef][PubMed]
75. Jørgensen MG,, Thomason MK,, Havelund J,, Valentin-Hansen P,, Storz G . 2013. Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev 27 : 1132 1145.[PubMed]
76. Thomason MK,, Fontaine F,, De Lay N,, Storz G . 2012. A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol 84 : 17 35.[PubMed]

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