A Small Regulatory RNA Generated from the 5' Untranslated Region Targets Gluconeogenesis in Species

Overview

Journal mSphere

Publisher American Society for Microbiology

Specialties Microbiology
Parasitology

Date 2021 Jun 30

PMID 34190585

Citations 5

Authors

Xing Luo

Marick Esberard

Philippe Bouloc

Annick Jacq

Affiliations

Soon will be listed here.

Abstract

Vsr217 is a small RNA from Vibrio tasmaniensis LGP32, a pathogen associated with mortality events affecting juvenile oysters. The gene is located within the 5' untranslated region (UTR) of , encoding the ATPase component of the maltose importer, and is conserved within the genus . In the presence of maltose, is regulated by MalT, the positive regulator of the maltose regulon. is required in for the full expression of . In addition, Vsr217 acts in to downregulate the expression of encoding fructose-1,6-bisphosphatase, an enzyme involved in gluconeogenesis. Thus, in the presence of maltose, the induction of Vsr217 is expected to promote glycolysis by negatively regulating the expression of a key enzyme of gluconeogenesis. Juvenile pacific oysters have been subject in recent years to summer mortality episodes with deep economic consequences. The pathogen Vibrio tasmaniensis has been associated with such mortality events. For bacterial pathogens, survival within the host requires profound metabolic adaptations according to available resources. All kinds of regulatory elements, including noncoding RNAs, orchestrate this response. Oysters are rich in glycogen, a precursor of maltose, and we previously reported that maltose-regulated genes are strongly induced during oyster infection. Here, we report the dual mechanism by which a small regulatory RNA, generated from the 5' untranslated region of a gene belonging to the maltose regulon, acts both in and . In , it stimulates growth on maltose, and in , it downregulates the expression of a gene associated with gluconeogenesis, thus coordinating maltose utilization with central carbon metabolism.

Citing Articles

outer membrane vesicles and infected cell exosomes: new players in host immune modulation and pathogenesis.

Wang X, Wang J, Mao L, Yao Y Front Immunol. 2024; 15:1512935.

PMID: 39726601 PMC: 11670821. DOI: 10.3389/fimmu.2024.1512935.

Rli51 Attenuates Transcription of the Pathogenicity Island 1 Gene and Functions as a -Acting sRNA in Intracellular Bacteria.

Moron A, Ortiz-Miravalles L, Penalver M, Garcia-Del Portillo F, Pucciarelli M, Ortega A Int J Mol Sci. 2024; 25(17).

PMID: 39273334 PMC: 11394854. DOI: 10.3390/ijms25179380.

Aminoglycoside uptake, stress, and potentiation in Gram-negative bacteria: new therapies with old molecules.

Lang M, Carvalho A, Baharoglu Z, Mazel D Microbiol Mol Biol Rev. 2023; 87(4):e0003622.

PMID: 38047635 PMC: 10732077. DOI: 10.1128/mmbr.00036-22.

Both extracellular vesicles from helicobacter pylori-infected cells and helicobacter pylori outer membrane vesicles are involved in gastric/extragastric diseases.

Wang C, Li W, Shao L, Zhou A, Zhao M, Li P Eur J Med Res. 2023; 28(1):484.

PMID: 37932800 PMC: 10626716. DOI: 10.1186/s40001-023-01458-z.

6S RNA-Dependent Susceptibility to RNA Polymerase Inhibitors.

Esberard M, Hallier M, Liu W, Morvan C, Bossi L, Figueroa-Bossi N Antimicrob Agents Chemother. 2022; 66(5):e0243521.

PMID: 35389235 PMC: 9112884. DOI: 10.1128/aac.02435-21.

References

Nguyen A, Disconzi E, Charriere G, Destoumieux-Garzon D, Bouloc P, Le Roux F . Gene Duplication Drives the Evolution of Redundant Regulatory Pathways Controlling Expression of the Major Toxic Secreted Metalloproteases in LGP32. mSphere. 2018; 3(6). PMC: 6262261. DOI: 10.1128/mSphere.00582-18. View

Vanhove A, Duperthuy M, Charriere G, Le Roux F, Goudenege D, Gourbal B . Outer membrane vesicles are vehicles for the delivery of Vibrio tasmaniensis virulence factors to oyster immune cells. Environ Microbiol. 2014; 17(4):1152-65. DOI: 10.1111/1462-2920.12535. View

Guo M, Updegrove T, Gogol E, Shabalina S, Gross C, Storz G . MicL, a new σE-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes Dev. 2014; 28(14):1620-34. PMC: 4102768. DOI: 10.1101/gad.243485.114. View

Melior H, Li S, Madhugiri R, Stotzel M, Azarderakhsh S, Barth-Weber S . Transcription attenuation-derived small RNA rnTrpL regulates tryptophan biosynthesis gene expression in trans. Nucleic Acids Res. 2019; 47(12):6396-6410. PMC: 6614838. DOI: 10.1093/nar/gkz274. View

Douchin V, Bohn C, Bouloc P . Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. J Biol Chem. 2006; 281(18):12253-9. DOI: 10.1074/jbc.M600819200. View

Schlegel A, Bohm A, Lee S, Peist R, Decker K, Boos W . Network regulation of the Escherichia coli maltose system. J Mol Microbiol Biotechnol. 2002; 4(3):301-7. View

Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, Cossart P . An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell. 2002; 110(5):551-61. DOI: 10.1016/s0092-8674(02)00905-4. View

Lakhal F, Bury-Mone S, Nomane Y, Le Goic N, Paillard C, Jacq A . DjlA, a membrane-anchored DnaJ-like protein, is required for cytotoxicity of clam pathogen Vibrio tapetis to hemocytes. Appl Environ Microbiol. 2008; 74(18):5750-8. PMC: 2547034. DOI: 10.1128/AEM.01043-08. View

Madeira F, Park Y, Lee J, Buso N, Gur T, Madhusoodanan N . The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 2019; 47(W1):W636-W641. PMC: 6602479. DOI: 10.1093/nar/gkz268. View

10.

Zhang Y, Yan D, Xia L, Zhao X, Osei-Adjei G, Xu S . The malS-5'UTR regulates hisG, a key gene in the histidine biosynthetic pathway in Salmonella enterica serovar Typhi. Can J Microbiol. 2017; 63(4):287-295. DOI: 10.1139/cjm-2016-0490. View

11.

Richet E, Raibaud O . Two MalT binding sites in direct repeat. A structural motif involved in the activation of all the promoters of the maltose regulons in Escherichia coli and Klebsiella pneumoniae. J Mol Biol. 1991; 218(2):323-34. DOI: 10.1016/0022-2836(91)90715-i. View

12.

Le Roux F, Binesse J, Saulnier D, Mazel D . Construction of a Vibrio splendidus mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector. Appl Environ Microbiol. 2006; 73(3):777-84. PMC: 1800747. DOI: 10.1128/AEM.02147-06. View

13.

Urban J, Vogel J . Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res. 2007; 35(3):1018-37. PMC: 1807950. DOI: 10.1093/nar/gkl1040. View

14.

Vanhove A, Rubio T, Nguyen A, Lemire A, Roche D, Nicod J . Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics. Environ Microbiol. 2015; 18(3):875-88. DOI: 10.1111/1462-2920.13083. View

15.

Loh E, Dussurget O, Gripenland J, Vaitkevicius K, Tiensuu T, Mandin P . A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell. 2009; 139(4):770-9. DOI: 10.1016/j.cell.2009.08.046. View

16.

Gottesman S, Storz G . Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol. 2010; 3(12). PMC: 3225950. DOI: 10.1101/cshperspect.a003798. View

17.

Wright P, Georg J, Mann M, Sorescu D, Richter A, Lott S . CopraRNA and IntaRNA: predicting small RNA targets, networks and interaction domains. Nucleic Acids Res. 2014; 42(Web Server issue):W119-23. PMC: 4086077. DOI: 10.1093/nar/gku359. View

18.

Gibson D . Enzymatic assembly of overlapping DNA fragments. Methods Enzymol. 2011; 498:349-61. PMC: 7149801. DOI: 10.1016/B978-0-12-385120-8.00015-2. View

19.

Gay M, Renault T, Pons A, Le Roux F . Two vibrio splendidus related strains collaborate to kill Crassostrea gigas: taxonomy and host alterations. Dis Aquat Organ. 2005; 62(1-2):65-74. DOI: 10.3354/dao062065. View

20.

Kawano M, Reynolds A, Miranda-Rios J, Storz G . Detection of 5'- and 3'-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res. 2005; 33(3):1040-50. PMC: 549416. DOI: 10.1093/nar/gki256. View