Bacterial small RNA

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Bacterial small RNAs are small RNAs produced by bacteria; they are 50- to 500-nucleotide non-coding RNA molecules, highly structured and containing several stem-loops. [1] [2] Numerous sRNAs have been identified using both computational analysis and laboratory-based techniques such as Northern blotting, microarrays and RNA-Seq [3] in a number of bacterial species including Escherichia coli , [4] [5] [6] the model pathogen Salmonella , [7] the nitrogen-fixing alphaproteobacterium Sinorhizobium meliloti , [8] marine cyanobacteria, [9] Francisella tularensis (the causative agent of tularaemia), [10] Streptococcus pyogenes [11] , the pathogen Staphylococcus aureus [12] , and the plant pathogen Xanthomonas oryzae pathovar oryzae. [13] Bacterial sRNAs affect how genes are expressed within bacterial cells via interaction with mRNA or protein, and thus can affect a variety of bacterial functions like metabolism, virulence, environmental stress response, and structure. [7] [12]

Contents

Origin

In the 1960s, the abbreviation sRNA was used to refer to "soluble RNA," which is now known as transfer RNA or tRNA (for an example of the abbreviation used in this sense, see [14] ). It is now known that most bacterial sRNAs are encoded by free-standing genes located in the intergenic regions (IGR) between two known genes. [3] [6] However, a class of sRNAs are shown to be derived from the 3'-UTR of mRNAs by independent transcription or nucleolytic cleavage. [15]

The first bacterial sRNA was discovered and characterized in 1984. [16] MicF in E. coli was found to regulate the expression of a key structural gene that makes up the outer membrane of the E. coli cell. [17] Shortly after, the Staphylococcus aureus sRNA RNAIII was found to act as a global regulator of S. aureus virulence and toxin secretion. [17] Since these initial discoveries, over six thousand bacterial sRNAs have been identified, largely through RNA-sequencing experiments. [18]

Techniques

Several laboratory and bioinformatic techniques can be used to identify and characterize sRNA transcripts. [3]

Function

Four common mechanisms of bacterial sRNA interaction with mRNA or protein targets. Bacterial small rna mechanisms.png
Four common mechanisms of bacterial sRNA interaction with mRNA or protein targets.

Bacterial sRNAs have a wide variety of regulatory mechanisms. Generally, sRNAs can bind to protein targets and modify the function of the bound protein. [22] Alternately, sRNAs may interact with mRNA targets and regulate gene expression by binding to complementary mRNA and blocking translation, or by unmasking or blocking the ribosome-binding site. [22]

sRNAs that interact with mRNA can also be categorized as cis- or trans-acting. Cis-acting sRNAs interact with genes encoded on the same genetic locus as the sRNA. [23] Some cis-acting sRNAs act as riboswitches, which have receptors for specific environmental or metabolic signals and activate or repress genes based on these signals. [17] Conversely, trans-encoded sRNAs interact with genes on separate loci. [1]

House-keeping

Amongst the targets of sRNAs are a number of house-keeping genes. The 6S RNA binds to RNA polymerase and regulates transcription, tmRNA has functions in protein synthesis, including the recycling of stalled ribosomes, 4.5S RNA regulates signal recognition particle (SRP), which is required for the secretion of proteins and RNase P is involved in maturing tRNAs. [24] [25]

Stress response

Many sRNAs are involved in stress response regulation. [26] They are expressed under stress conditions such as cold shock, iron depletion, onset of the SOS response and sugar stress. [25] The small RNA ryfA has been found to affect the stress response of uropathogenic E.coli, under osmotic and oxidative stress. [27] The small RNA nitrogen stress-induced RNA 1 (NsiR1) is produced by Cyanobacteria under conditions of nitrogen deprivation. [28] Cyanobacteria NisR8 and NsiR9 sRNAs could be related to the differentiation of nitrogen-fixing cells (heterocysts). [29]

Regulation of RpoS

The RpoS gene in E. coli encodes sigma 38, a sigma factor which regulates stress response and acts as a transcriptional regulator for many genes involved in cell adaptation. At least three sRNAs, DsrA, RprA and OxyS, regulate the translation of RpoS. DsrA and RprA both activate RpoS translation by base pairing to a region in the leader sequence of the RpoS mRNA and disrupting formation of a hairpin which frees up the ribosome loading site. OxyS inhibits RpoS translation. DsrA levels are increased in response to low temperatures and osmotic stress, and RprA levels are increased in response to osmotic stress and cell-surface stress, therefore increasing RpoS levels in response to these conditions. Levels of OxyS are increased in response to oxidative stress, therefore inhibiting RpoS under these conditions. [25] [30] [31]

Regulation of outer membrane proteins

The outer membrane of gram negative bacteria acts as a barrier to prevent the entry of toxins into the bacterial cell, and plays a role in the survival of bacterial cells in diverse environments. Outer membrane proteins (OMPs) include porins and adhesins. Numerous sRNAs regulate the expression of OMPs. The porins OmpC and OmpF are responsible for the transport of metabolites and toxins. The expression of OmpC and OmpF is regulated by the sRNAs MicC and MicF in response to stress conditions. [32] [33] [34] The outer membrane protein OmpA anchors the outer membrane to the murein layer of the periplasmic space. Its expression is downregulated in the stationary phase of cell-growth. In E. coli the sRNA MicA depletes OmpA levels, in Vibrio cholerae the sRNA VrrA represses synthesis of OmpA in response to stress. [32] [35]

Virulence

In some bacteria sRNAs regulate virulence genes. In Salmonella , the pathogenicity island encoded InvR RNA represses synthesis of the major outer membrane protein OmpD; another co-activated DapZ sRNA from 3'-UTR represses abundant membrane Opp/Dpp transporters of oligopeptides; [15] and SgrS sRNA regulates the expression of the secreted effector protein SopD. [7] In Staphylococcus aureus , RNAIII regulates a number of genes involved in toxin and enzyme production and cell-surface proteins. [25] The FasX sRNA is the only well-characterized regulatory RNA known to control the regulation of several virulence factors in Streptococcus pyogenes , including both cell-surface associated adhesion proteins as well as secreted factors. [36] [37] [38] [39]

Quorum sensing

In Vibrio species, the Qrr sRNAs and the chaperone protein Hfq are involved in the regulation of quorum sensing. Qrr sRNAs regulate the expression of several mRNAs including the quorum-sensing master regulators LuxR and HapR. [40] [41]

Biofilm Formation

Biofilm is a type of bacterial growth pattern where multiple layers of bacterial cells adhere to a host surface. This mode of growth is often found in pathogenic bacteria, including Pseudomonas aeruginosa , which can form persistent biofilm within the respiratory tract and cause chronic infection. [42] The P. aeruginosa sRNA SbrA was found to be necessary for full biofilm formation and pathogenicity. [42] A mutant P. aeruginosa strain with SbrA deleted formed a 66% smaller biofilm and its ability to infect a nematode model was reduced by nearly half when compared to wildtype P. aeruginosa. [42]

Antibiotic Resistance

Several bacterial sRNAs are involved in the regulation of genes that confer antibiotic resistance. [43] For example, the sRNA DsrA regulates a drug efflux pump in E. coli, which is a system that mechanically pumps antibiotic out of bacterial cells. [43] E. coli MicF also contributes to antibiotic resistance of cephalosporins, as it regulates membrane proteins involved in uptake of these class of antibiotics. [43]

Target prediction

In order to understand an sRNA's function one primarily needs to describe its targets. Here, target predictions represent a fast and free method for initial characterization of putative targets, given that the sRNA actually exerts its function via direct base pairing with a target RNA. Examples are CopraRNA, [44] [45] IntaRNA, [45] [46] [47] TargetRNA [20] and RNApredator. [48] It has been shown that target prediction for enterobacterial sRNAs can benefit from transcriptome wide Hfq-binding maps. [49]

Databases

See also

Related Research Articles

The gene rpoS encodes the sigma factor sigma-38, a 37.8 kD protein in Escherichia coli. Sigma factors are proteins that regulate transcription in bacteria. Sigma factors can be activated in response to different environmental conditions. rpoS is transcribed in late exponential phase, and RpoS is the primary regulator of stationary phase genes. RpoS is a central regulator of the general stress response and operates in both a retroactive and a proactive manner: it not only allows the cell to survive environmental challenges, but it also prepares the cell for subsequent stresses (cross-protection). The transcriptional regulator CsgD is central to biofilm formation, controlling the expression of the curli structural and export proteins, and the diguanylate cyclase, adrA, which indirectly activates cellulose production. The rpoS gene most likely originated in the gammaproteobacteria.

In molecular genetics, a regulon is a group of genes that are regulated as a unit, generally controlled by the same regulatory gene that expresses a protein acting as a repressor or activator. This terminology is generally, although not exclusively, used in reference to prokaryotes, whose genomes are often organized into operons; the genes contained within a regulon are usually organized into more than one operon at disparate locations on the chromosome. Applied to eukaryotes, the term refers to any group of non-contiguous genes controlled by the same regulatory gene.

fis E. coli gene

fis is an E. coli gene encoding the Fis protein. The regulation of this gene is more complex than most other genes in the E. coli genome, as Fis is an important protein which regulates expression of other genes. It is supposed that fis is regulated by H-NS, IHF and CRP. It also regulates its own expression (autoregulation). Fis is one of the most abundant DNA binding proteins in Escherichia coli under nutrient-rich growth conditions.

<span class="mw-page-title-main">DicF RNA</span> Non-coding RNA

DicF RNA is a non-coding RNA that is an antisense inhibitor of cell division gene ftsZ. DicF is bound by the Hfq protein which enhances its interaction with its targets. Pathogenic E. coli strains possess multiple copies of sRNA DicF in their genomes, while non-pathogenic strains do not. DicF and Hfq are both necessary to reduce FtsZ protein levels, leading to cell filamentation under anaerobic conditions.

<span class="mw-page-title-main">DsrA RNA</span> Non-coding RNA

DsrA RNA is a non-coding RNA that regulates both transcription, by overcoming transcriptional silencing by the nucleoid-associated H-NS protein, and translation, by promoting efficient translation of the stress sigma factor, RpoS. These two activities of DsrA can be separated by mutation: the first of three stem-loops of the 85 nucleotide RNA is necessary for RpoS translation but not for anti-H-NS action, while the second stem-loop is essential for antisilencing and less critical for RpoS translation. The third stem-loop, which behaves as a transcription terminator, can be substituted by the trp transcription terminator without loss of either DsrA function. The sequence of the first stem-loop of DsrA is complementary with the upstream leader portion of RpoS messenger RNA, suggesting that pairing of DsrA with the RpoS message might be important for translational regulation. The structures of DsrA and DsrA/rpoS complex were studied by NMR. The study concluded that the sRNA contains a dynamic conformational equilibrium for its second stem–loop which might be an important mechanism for DsrA to regulate the translations of its multiple target mRNAs.

<span class="mw-page-title-main">GcvB RNA</span>

The gcvB RNA gene encodes a small non-coding RNA involved in the regulation of a number of amino acid transport systems as well as amino acid biosynthetic genes. The GcvB gene is found in enteric bacteria such as Escherichia coli. GcvB regulates genes by acting as an antisense binding partner of the mRNAs for each regulated gene. This binding is dependent on binding to a protein called Hfq. Transcription of the GcvB RNA is activated by the adjacent GcvA gene and repressed by the GcvR gene. A deletion of GcvB RNA from Y. pestis changed colony shape as well as reducing growth. It has been shown by gene deletion that GcvB is a regulator of acid resistance in E. coli. GcvB enhances the ability of the bacterium to survive low pH by upregulating the levels of the alternate sigma factor RpoS. A polymeric form of GcvB has recently been identified. Interaction of GcvB with small RNA SroC triggers the degradation of GcvB by RNase E, lifting the GcvB-mediated mRNA repression of its target genes.

<span class="mw-page-title-main">OmrA-B RNA</span>

The OmrA-B RNA gene family is a pair of homologous OmpR-regulated small non-coding RNA that was discovered in E. coli during two large-scale screens. OmrA-B is highly abundant in stationary phase, but low levels could be detected in exponentially growing cells as well. RygB is adjacent to RygA a closely related RNA. These RNAs bind to the Hfq protein and regulate gene expression by antisense binding. They negatively regulate the expression of several genes encoding outer membrane proteins, including cirA, CsgD, fecA, fepA and ompT by binding in the vicinity of the Shine-Dalgarno sequence, suggesting the control of these targets is dependent on Hfq protein and RNase E. Taken together, these data suggest that OmrA-B participates in the regulation of outer membrane composition, responding to environmental conditions.

<span class="mw-page-title-main">MicF RNA</span> Gene found in bacteria

The micF RNA is a non-coding RNA stress response gene found in Escherichia coli and related bacteria that post-transcriptionally controls expression of the outer membrane porin gene ompF. The micF gene encodes a non-translated 93 nucleotide antisense RNA that binds its target ompF mRNA and regulates ompF expression by inhibiting translation and inducing degradation of the message. In addition, other factors, such as the RNA chaperone protein StpA also play a role in this regulatory system. The expression of micF is controlled by both environmental and internal stress factors. Four transcriptional regulators are known to bind the micF promoter region and activate micF expression.

<span class="mw-page-title-main">OxyS RNA</span>

OxyS RNA is a small non-coding RNA which is induced in response to oxidative stress in Escherichia coli. This RNA acts as a global regulator to activate or repress the expression of as many as 40 genes, by an antisense mechanism, including the fhlA-encoded transcriptional activator and the rpoS-encoded sigma(s) subunit of RNA polymerase. OxyS is bound by the Hfq protein, that increases the OxyS RNA interaction with its target messages. Binding to Hfq alters the conformation of OxyS. The 109 nucleotide RNA is thought to be composed of three stem-loops.

<span class="mw-page-title-main">RprA RNA</span>

The RprA RNA gene encodes a 106 nucleotide regulatory non-coding RNA. Translational regulation of the stationary phase sigma factor RpoS is mediated by the formation of a double-stranded RNA stem-loop structure in the upstream region of the rpoS messenger RNA, occluding the translation initiation site.

<span class="mw-page-title-main">RyhB</span> 90 nucleotide RNA

RyhB RNA is a 90 nucleotide RNA that down-regulates a set of iron-storage and iron-using proteins when iron is limiting; it is itself negatively regulated by the ferric uptake repressor protein, Fur.

<span class="mw-page-title-main">MicA RNA</span>

The MicA RNA is a small non-coding RNA that was discovered in E. coli during a large scale screen. Expression of SraD is highly abundant in stationary phase, but low levels could be detected in exponentially growing cells as well.

<span class="mw-page-title-main">ArcZ RNA</span>

In molecular biology the ArcZ RNA is a small non-coding RNA (ncRNA). It is the functional product of a gene which is not translated into protein. ArcZ is an Hfq binding RNA that functions as an antisense regulator of a number of protein coding genes.

<span class="mw-page-title-main">Hfq protein</span>

The Hfq protein encoded by the hfq gene was discovered in 1968 as an Escherichia coli host factor that was essential for replication of the bacteriophage Qβ. It is now clear that Hfq is an abundant bacterial RNA binding protein which has many important physiological roles that are usually mediated by interacting with Hfq binding sRNA.

<span class="mw-page-title-main">Invasion gene associated RNA</span>

Invasion gene associated RNA is a small non-coding RNA involved in regulating one of the major outer cell membrane porin proteins in Salmonella species.

<span class="mw-page-title-main">Vibrio regulatory RNA of OmpA</span>

VrrA is a non-coding RNA that is conserved across all Vibrio species of bacteria and acts as a repressor for the synthesis of the outer membrane protein OmpA. This non-coding RNA was initially identified from Tn5 transposon mutant libraries of Vibrio cholerae and its location within the bacterial genome was mapped to the intergenic region between genes VC1741 and VC1743 by RACE analysis.

In molecular biology, the FasX small RNA (fibronectin/fibrinogen-binding/haemolytic-activity/streptokinase-regulator-X) is a non-coding small RNA (sRNA) produced by all group A Streptococcus. FasX has also been found in species of group D and group G Streptococcus. FasX regulates expression of secreted virulence factor streptokinase (SKA), encoded by the ska gene. FasX base pairs to the 5' end of the ska mRNA, increasing the stability of the mRNA, resulting in elevated levels of streptokinase expression. FasX negatively regulates the expression of pili and fibronectin-binding proteins on the bacterial cell surface. It binds to the 5' untranslated region of genes in the FCT-region in a serotype-specific manner, reducing the stability of and inhibiting translation of the pilus biosynthesis operon mRNA by occluding the ribosome-binding site through a simple Watson-Crick base-pairing mechanism.

The gene rpoN encodes the sigma factor sigma-54, a protein in Escherichia coli and other species of bacteria. RpoN antagonizes RpoS sigma factors.

Bacterial small RNAs (sRNA) are an important class of regulatory molecules in bacteria such as Brucella. They are often bound to the chaperone protein Hfq, which allows them to interact with mRNA(s). In Brucella suis 1330 RNA sequencing identified a novel list of 33 sRNAs and 62 Hfq-associated mRNAs. In Brucella melitensis eight novel sRNA genes were identified using bioinformatic and experimental approach. One of them BSR0602 was found to modulate the intracellular survival of B. melitensis. In another large-scale deep sequencing study 1321 sRNAs were identified in B. melitensis. BSR0441 sRNA was further investigated in this study and shown to play role in the intracellular survival. sRNA BM-sr0117 from Brucella melitensis was identified and shown to be bound to and cleaved by Bm-RNase III. AbcR and AbcR2 were studied B. abortus. Seven novel sRNAs were validated and their interaction with a putative target sequence was verified in B. abortus.

<span class="mw-page-title-main">Anti small RNA</span> RNA sequences

Antisense small RNAs are short RNA sequences that are complementary to other small RNA (sRNA) in the cell.

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