The Small RNA NcS25 Regulates Biological Amine-Transporting Outer Membrane Porin BCAL3473 in Burkholderia Cenocepacia

Overview

Journal mSphere

Publisher American Society for Microbiology

Specialties Microbiology
Parasitology

Date 2023 Mar 27

PMID 36971554

Authors

Andrea M Sass

Tom Coenye

Affiliations

Soon will be listed here.

Abstract

Regulation of porin expression in bacteria is complex and often involves small-RNA regulators. Several small-RNA regulators have been described for Burkholderia cenocepacia, and this study aimed to characterize the biological role of the conserved small RNA NcS25 and its cognate target, outer membrane protein BCAL3473. The B. cenocepacia genome carries a large number of genes encoding porins with yet-uncharacterized functions. Expression of the porin BCAL3473 is strongly repressed by NcS25 and activated by other factors, such as a LysR-type regulator and nitrogen-depleted growth conditions. The porin is involved in transport of arginine, tyrosine, tyramine, and putrescine across the outer membrane. Porin BCAL3473, with NcS25 as a major regulator, plays an important role in the nitrogen metabolism of B. cenocepacia. Burkholderia cenocepacia is a Gram-negative bacterium which causes infections in immunocompromised individuals and in people with cystic fibrosis. A low outer membrane permeability is one of the factors giving it a high level of innate resistance to antibiotics. Porins provide selective permeability for nutrients, and antibiotics can also traverse the outer membrane by this means. Knowing the properties and specificities of porin channels is therefore important for understanding resistance mechanisms and for developing new antibiotics and could help in overcoming permeability issues in antibiotic treatment.

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References

de la Cruz M, Calva E . The complexities of porin genetic regulation. J Mol Microbiol Biotechnol. 2010; 18(1):24-36. DOI: 10.1159/000274309. View

Pusic P, Sonnleitner E, Blasi U . Specific and Global RNA Regulators in . Int J Mol Sci. 2021; 22(16). PMC: 8395346. DOI: 10.3390/ijms22168632. View

Figurski D, Helinski D . Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A. 1979; 76(4):1648-52. PMC: 383447. DOI: 10.1073/pnas.76.4.1648. View

Sugawara E, Nikaido H . OmpA is the principal nonspecific slow porin of Acinetobacter baumannii. J Bacteriol. 2012; 194(15):4089-96. PMC: 3416538. DOI: 10.1128/JB.00435-12. View

Chevalier S, Bouffartigues E, Bodilis J, Maillot O, Lesouhaitier O, Feuilloley M . Structure, function and regulation of Pseudomonas aeruginosa porins. FEMS Microbiol Rev. 2017; 41(5):698-722. DOI: 10.1093/femsre/fux020. View

Cardona S, Valvano M . An expression vector containing a rhamnose-inducible promoter provides tightly regulated gene expression in Burkholderia cenocepacia. Plasmid. 2005; 54(3):219-28. DOI: 10.1016/j.plasmid.2005.03.004. View

Parr Jr T, Moore R, Moore L, Hancock R . Role of porins in intrinsic antibiotic resistance of Pseudomonas cepacia. Antimicrob Agents Chemother. 1987; 31(1):121-3. PMC: 174667. DOI: 10.1128/AAC.31.1.121. View

Bush M, Dixon R . The role of bacterial enhancer binding proteins as specialized activators of σ54-dependent transcription. Microbiol Mol Biol Rev. 2012; 76(3):497-529. PMC: 3429621. DOI: 10.1128/MMBR.00006-12. View

Mahenthiralingam E, Baldwin A, Dowson C . Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol. 2008; 104(6):1539-51. DOI: 10.1111/j.1365-2672.2007.03706.x. View

10.

Valentin-Hansen P, Johansen J, Rasmussen A . Small RNAs controlling outer membrane porins. Curr Opin Microbiol. 2007; 10(2):152-5. DOI: 10.1016/j.mib.2007.03.001. View

11.

Morita T, Aiba H . RNase E action at a distance: degradation of target mRNAs mediated by an Hfq-binding small RNA in bacteria. Genes Dev. 2011; 25(4):294-8. PMC: 3042153. DOI: 10.1101/gad.2030311. View

12.

Papenfort K, Bouvier M, Mika F, Sharma C, Vogel J . Evidence for an autonomous 5' target recognition domain in an Hfq-associated small RNA. Proc Natl Acad Sci U S A. 2010; 107(47):20435-40. PMC: 2996696. DOI: 10.1073/pnas.1009784107. View

13.

Compant S, Nowak J, Coenye T, Clement C, Barka E . Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev. 2008; 32(4):607-26. DOI: 10.1111/j.1574-6976.2008.00113.x. View

14.

Baugh L, Gallagher L, Patrapuvich R, Clifton M, Gardberg A, Edwards T . Combining functional and structural genomics to sample the essential Burkholderia structome. PLoS One. 2013; 8(1):e53851. PMC: 3561365. DOI: 10.1371/journal.pone.0053851. View

15.

Lorenz R, Bernhart S, Honer Zu Siederdissen C, Tafer H, Flamm C, Stadler P . ViennaRNA Package 2.0. Algorithms Mol Biol. 2011; 6:26. PMC: 3319429. DOI: 10.1186/1748-7188-6-26. View

16.

Sass A, Van Acker H, Forstner K, Van Nieuwerburgh F, Deforce D, Vogel J . Genome-wide transcription start site profiling in biofilm-grown Burkholderia cenocepacia J2315. BMC Genomics. 2015; 16:775. PMC: 4603805. DOI: 10.1186/s12864-015-1993-3. View

17.

Lalaouna D, Simoneau-Roy M, Lafontaine D, Masse E . Regulatory RNAs and target mRNA decay in prokaryotes. Biochim Biophys Acta. 2013; 1829(6-7):742-7. DOI: 10.1016/j.bbagrm.2013.02.013. View

18.

Gonyar L, Fankhauser S, Goldberg J . Single amino acid substitution in homogentisate 1,2-dioxygenase is responsible for pigmentation in a subset of Burkholderia cepacia complex isolates. Environ Microbiol Rep. 2014; 7(2):180-7. PMC: 4560265. DOI: 10.1111/1758-2229.12217. View

19.

Higgins S, Sanchez-Contreras M, Gualdi S, Pinto-Carbo M, Carlier A, Eberl L . The Essential Genome of Burkholderia cenocepacia H111. J Bacteriol. 2017; 199(22). PMC: 5648868. DOI: 10.1128/JB.00260-17. View

20.

Liu Y, Lardi M, Pedrioli A, Eberl L, Pessi G . NtrC-dependent control of exopolysaccharide synthesis and motility in Burkholderia cenocepacia H111. PLoS One. 2017; 12(6):e0180362. PMC: 5491218. DOI: 10.1371/journal.pone.0180362. View