Small RNAs regulating biofilm formation and outer membrane homeostasis

Nowadays, the identification of small non-coding RNAs takes a prominent role in deciphering complex bacterial phenotypes. Evidences are given that the post-transcriptional layer of regulation mediated by sRNAs plays an important role in the formation of bacterial biofilms. These sRNAs exert their activity on various targets, be it directly or indirectly linked to biofilm formation. First, and best described, are the sRNAs that act in core regulatory pathways of biofilm formation, such as those regulating motility and matrix production. Second, overlaps between the regulation of biofilm formation and the outer membrane (OM) are becoming obvious. Additionally, different studies indicate that defects in the OM itself affect biofilm formation through this shared cascade, thereby forming a feedback mechanism. Interestingly, it is known that the OM itself is extensively regulated by different sRNAs. Third, biofilms are also linked to global metabolic changes. There is also evidence that metabolic pathways and the process of biofilm formation share sRNAs.

[1]  Raju Tomer,et al.  A small non‐coding RNA of the invasion gene island (SPI‐1) represses outer membrane protein synthesis from the Salmonella core genome , 2007, Molecular microbiology.

[2]  G. Storz,et al.  Regulatory RNAs in Bacteria , 2009, Cell.

[3]  U. Römling,et al.  Regulation of Biofilm Components in Salmonella enterica Serovar Typhimurium by Lytic Transglycosylases Involved in Cell Wall Turnover , 2011, Journal of bacteriology.

[4]  N. Delihas,et al.  Secondary structures of Escherichia coli antisense micF RNA, the 5'-end of the target ompF mRNA, and the RNA/RNA duplex. , 1995, Biochemistry.

[5]  J. Vogel,et al.  Systematic deletion of Salmonella small RNA genes identifies CyaR, a conserved CRP‐dependent riboregulator of OmpX synthesis , 2008, Molecular microbiology.

[6]  H. Margalit,et al.  Novel small RNA-encoding genes in the intergenic regions of Escherichia coli , 2001, Current Biology.

[7]  J. Gunn,et al.  Comparative Analysis of Salmonella enterica Serovar Typhimurium Biofilm Formation on Gallstones and on Glass , 2003, Infection and Immunity.

[8]  J. Vanderleyden,et al.  Salmonella biofilms: An overview on occurrence, structure, regulation and eradication , 2012 .

[9]  T. Wood,et al.  Hha, YbaJ, and OmpA regulate Escherichia coli K12 biofilm formation and conjugation plasmids abolish motility , 2006, Biotechnology and bioengineering.

[10]  K. Marchal,et al.  The small regulatory RNA molecule MicA is involved in Salmonella enterica serovar Typhimurium biofilm formation , 2010, BMC Microbiology.

[11]  Qun Ma,et al.  OmpA influences Escherichia coli biofilm formation by repressing cellulose production through the CpxRA two-component system. , 2009, Environmental microbiology.

[12]  M. Inouye,et al.  Phosphorylation of OmpR by the osmosensor EnvZ modulates expression of the ompF and ompC genes in Escherichia coli. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[13]  S. Gottesman,et al.  MicA sRNA links the PhoP regulon to cell envelope stress , 2010, Molecular microbiology.

[14]  N. Majdalani,et al.  Bacterial Small RNA Regulators , 2005, Critical reviews in biochemistry and molecular biology.

[15]  G. Storz,et al.  The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF‐I) protein , 1998, The EMBO journal.

[16]  G. Storz,et al.  A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli , 2012, Molecular microbiology.

[17]  S. Gottesman,et al.  Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA , 2010, The EMBO journal.

[18]  G. Storz,et al.  Identification of novel small RNAs using comparative genomics and microarrays. , 2001, Genes & development.

[19]  E. Wagner,et al.  Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis , 2010, The EMBO journal.

[20]  L. Bossi,et al.  Caught at its own game: regulatory small RNA inactivated by an inducible transcript mimicking its target. , 2009, Genes & development.

[21]  J. Vogel,et al.  σE-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay , 2006, Molecular microbiology.

[22]  K. Udekwu.  Transcriptional and Post-Transcriptional Regulation of the Escherichia coli luxS mRNA; Involvement of the sRNA MicA , 2010, PloS one.

[23]  J. Vogel,et al.  Pervasive post‐transcriptional control of genes involved in amino acid metabolism by the Hfq‐dependent GcvB small RNA , 2011, Molecular microbiology.

[24]  J. Vogel,et al.  Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation , 2009, Nature Structural &Molecular Biology.

[25]  S. Gottesman,et al.  The 5′ end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator , 2008, Nucleic acids research.

[26]  N. Majdalani,et al.  Regulation of RpoS by a novel small RNA: the characterization of RprA. , 2001, Molecular microbiology.

[27]  C. K. Vanderpool,et al.  The small RNA SgrS controls sugar–phosphate accumulation by regulating multiple PTS genes , 2011, Nucleic acids research.

[28]  L. Bossi,et al.  Recognition of heptameric seed sequence underlies multi‐target regulation by RybB small RNA in Salmonella enterica , 2010, Molecular microbiology.

[29]  P. Lejeune,et al.  The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? , 2006, Research in microbiology.

[30]  S. Gottesman,et al.  The Crp-Activated Small Noncoding Regulatory RNA CyaR (RyeE) Links Nutritional Status to Group Behavior , 2008, Journal of bacteriology.

[31]  Jörg Vogel,et al.  Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon , 2011, Proceedings of the National Academy of Sciences.

[32]  Jörg Vogel,et al.  A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD , 2011, Nucleic acids research.

[33]  P. Bouloc,et al.  Down-regulation of Porins by a Small RNA Bypasses the Essentiality of the Regulated Intramembrane Proteolysis Protease RseP in Escherichia coli* , 2006, Journal of Biological Chemistry.

[34]  P. Vuong,et al.  Novel Mechanism of Escherichia coli Porin Regulation , 2006, Journal of bacteriology.

[35]  Erik Holmqvist,et al.  A mixed double negative feedback loop between the sRNA MicF and the global regulator Lrp , 2012, Molecular microbiology.

[36]  J. Vogel,et al.  Small non-coding RNAs and the bacterial outer membrane. , 2006, Current opinion in microbiology.

[37]  J. Vogel,et al.  Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. , 2005, Genes & development.

[38]  H. Lappin-Scott,et al.  The transcriptional programme of Salmonella enterica serovar Typhimurium reveals a key role for tryptophan metabolism in biofilms , 2009, BMC Genomics.

[39]  S. Gottesman,et al.  A complex network of small non‐coding RNAs regulate motility in Escherichia coli , 2012, Molecular microbiology.

[40]  M. Surette,et al.  A Global Metabolic Shift Is Linked to Salmonella Multicellular Development , 2010, PloS one.

[41]  Regine Hengge,et al.  'Life-style' control networks in Escherichia coli: signaling by the second messenger c-di-GMP. , 2012, Journal of biotechnology.

[42]  P. Valentin‐Hansen,et al.  Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase‐dependent control , 2005, Molecular microbiology.

[43]  N. Majdalani,et al.  DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[44]  G. Storz,et al.  Modulating the outer membrane with small RNAs. , 2006, Genes & development.

[45]  H. Mori,et al.  A Genome-wide Approach to Identify the Genes Involved in Biofilm Formation in E. coli , 2008, DNA research : an international journal for rapid publication of reports on genes and genomes.

[46]  Pimlapas Leekitcharoenphon,et al.  The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium , 2012, Proceedings of the National Academy of Sciences.

[47]  J. Vogel,et al.  Small RNA binding to 5' mRNA coding region inhibits translational initiation. , 2008, Molecular cell.

[48]  G. Storz,et al.  MicC, a Second Small-RNA Regulator of Omp Protein Expression in Escherichia coli , 2004, Journal of bacteriology.

[49]  Jay C D Hinton,et al.  Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA , 2012, Molecular microbiology.

[50]  B. Kallipolitis,et al.  A conserved small RNA promotes silencing of the outer membrane protein YbfM , 2009, Molecular microbiology.

[51]  L. Bossi,et al.  A small RNA downregulates LamB maltoporin in Salmonella , 2007, Molecular microbiology.

[52]  S. Gottesman,et al.  Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs , 2006, Molecular microbiology.

[53]  N. Majdalani,et al.  Mechanism of Positive Regulation by DsrA and RprA Small Noncoding RNAs: Pairing Increases Translation and Protects rpoS mRNA from Degradation , 2010, Journal of bacteriology.

[54]  C. Solano,et al.  Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose , 2002, Molecular microbiology.

[55]  N. Majdalani,et al.  The Rcs phosphorelay: a complex signal transduction system. , 2005, Annual review of microbiology.

[56]  W. B. Snyder,et al.  Mutational activation of the Cpx signal transduction pathway of Escherichia coli suppresses the toxicity conferred by certain envelope‐associated stresses , 1995, Molecular microbiology.

[57]  P. Valentin‐Hansen,et al.  Conserved small non-coding RNAs that belong to the sigmaE regulon: role in down-regulation of outer membrane proteins. , 2006, Journal of molecular biology.

[58]  N. Majdalani,et al.  Regulation of RpoS by a novel small RNA: the characterization of RprA , 2001 .

[59]  J. Gunn,et al.  Flagellated but Not Hyperfimbriated Salmonella enterica Serovar Typhimurium Attaches to and Forms Biofilms on Cholesterol-Coated Surfaces , 2010, Journal of bacteriology.

[60]  B. Kallipolitis,et al.  Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and sigmaE-dependent CyaR-ompX regulatory case. , 2008, Journal of molecular biology.

[61]  L. Wang,et al.  Outer membrane defect and stronger biofilm formation caused by inactivation of a gene encoding for heptosyltransferase I in Cronobacter sakazakii ATCC BAA‐894 , 2012, Journal of applied microbiology.

[62]  G. Storz,et al.  The base-pairing RNA spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli. , 2011, Molecular cell.

[63]  P. Valentin‐Hansen,et al.  Small regulatory RNAs control the multi‐cellular adhesive lifestyle of Escherichia coli , 2012, Molecular microbiology.

[64]  M. Malcova,et al.  aroA and aroD mutations influence biofilm formation in Salmonella Enteritidis. , 2009, FEMS microbiology letters.

[65]  Regine Hengge,et al.  Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli , 2012, Molecular microbiology.

[66]  K. Hentrich,et al.  Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar Typhimurium , 2012, RNA biology.