Abstract
HmsB, a temperature-dependent sRNA, promotes biofilm formation by Yersinia pestis, but whether its own expression is regulated by other regulators is still poorly understood. RovM is a global regulator that activates biofilm formation but represses the virulence of Y. pestis. In this work, the results of primer extension, quantitative real-time PCR (qRT-PCR), and LacZ fusion demonstrated that RovM was able to activate hmsB expression. However, the results of electrophoretic mobility shift assay (EMSA) showed that His-RovM did not bind to the upstream DNA region of hmsB. Thus, RovM may exert its regulatory action on hmsB expression in an indirect manner. The data presented here enriched the content of the regulatory circuits that control gene expression in Y. pestis.
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References
Barbieri R, Signoli M, Cheve D, Costedoat C, Tzortzis S, Aboudharam G, Raoult D, Drancourt M (2020) Yersinia pestis: the natural history of plague. Clin Microbiol Rev. https://doi.org/10.1128/CMR.00044-19
He Z, Wei B, Zhang Y, Liu J, Xi J, Ciren D, Qi T, Liang J, Duan R, Qin S, Lv D, Chen Y, Xiao M, Fan R, Song Z, Jing H, Wang X (2021) Distribution and characteristics of human plague cases and Yersinia pestis isolates from 4 marmota plague Foci, China, 1950–2019. Emerg Infect Dis 27(10):2544–2553. https://doi.org/10.3201/eid2710.202239
Zhou D, Yang R (2011) Formation and regulation of Yersinia biofilms. Protein Cell 2(3):173–179. https://doi.org/10.1007/s13238-011-1024-3
Bobrov AG, Kirillina O, Forman S, Mack D, Perry RD (2008) Insights into Yersinia pestis biofilm development: topology and co-interaction of Hms inner membrane proteins involved in exopolysaccharide production. Environ Microbiol 10(6):1419–1432. https://doi.org/10.1111/j.1462-2920.2007.01554.x
Gahlot DK, Wai SN, Erickson DL, Francis MS (2022) Cpx-signalling facilitates Hms-dependent biofilm formation by Yersinia pseudotuberculosis. NPJ Biofilms Microbiomes 8(1):13. https://doi.org/10.1038/s41522-022-00281-4
Bobrov AG, Kirillina O, Ryjenkov DA, Waters CM, Price PA, Fetherston JD, Mack D, Goldman WE, Gomelsky M, Perry RD (2011) Systematic analysis of cyclic di-GMP signalling enzymes and their role in biofilm formation and virulence in Yersinia pestis. Mol Microbiol 79(2):533–551. https://doi.org/10.1111/j.1365-2958.2010.07470.x
Sun YC, Koumoutsi A, Jarrett C, Lawrence K, Gherardini FC, Darby C, Hinnebusch BJ (2011) Differential control of Yersinia pestis biofilm formation in vitro and in the flea vector by two c-di-GMP diguanylate cyclases. PLoS One 6(4):e19267. https://doi.org/10.1371/journal.pone.0019267
Heroven AK, Dersch P (2006) RovM, a novel LysR-type regulator of the virulence activator gene rovA, controls cell invasion, virulence and motility of Yersinia pseudotuberculosis. Mol Microbiol 62(5):1469–1483. https://doi.org/10.1111/j.1365-2958.2006.05458.x
Liu L, Fang H, Yang H, Zhang Y, Han Y, Zhou D, Yang R (2016) Reciprocal regulation of Yersinia pestis biofilm formation and virulence by RovM and RovA. Open Biol. https://doi.org/10.1098/rsob.150198
Cathelyn JS, Crosby SD, Lathem WW, Goldman WE, Miller VL (2006) RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc Natl Acad Sci U S A 103(36):13514–13519. https://doi.org/10.1073/pnas.0603456103
Vadyvaloo V, Hinz AK (2015) A LysR-type transcriptional regulator, RovM, senses nutritional cues suggesting that it is involved in metabolic adaptation of Yersinia pestis to the flea gut. PLoS One 10(9):e0137508. https://doi.org/10.1371/journal.pone.0137508
Thanikkal EJ, Gahlot DK, Liu J, Fredriksson Sundbom M, Gurung JM, Ruuth K, Francis MK, Obi IR, Thompson KM, Chen S, Dersch P, Francis MS (2019) The Yersinia pseudotuberculosis Cpx envelope stress system contributes to transcriptional activation of rovM. Virulence 10(1):37–57. https://doi.org/10.1080/21505594.2018.1556151
Yan Y, Su S, Meng X, Ji X, Qu Y, Liu Z, Wang X, Cui Y, Deng Z, Zhou D, Jiang W, Yang R, Han Y (2013) Determination of sRNA expressions by RNA-seq in Yersinia pestis grown in vitro and during infection. PLoS One 8(9):e74495. https://doi.org/10.1371/journal.pone.0074495
Fang N, Qu S, Yang H, Fang H, Liu L, Zhang Y, Wang L, Han Y, Zhou D, Yang R (2014) HmsB enhances biofilm formation in Yersinia pestis. Front Microbiol 5:685. https://doi.org/10.3389/fmicb.2014.00685
Liu L, He Y, Yang H, Liu W, Zheng S, Qi Y, Zhou D, Zhang Y, Yin Z (2022) Nlp enhances biofilm formation by Yersinia pestis biovar microtus. Microb Pathog 169:105659. https://doi.org/10.1016/j.micpath.2022.105659
Zhou D, Tong Z, Song Y, Han Y, Pei D, Pang X, Zhai J, Li M, Cui B, Qi Z, Jin L, Dai R, Du Z, Wang J, Guo Z, Wang J, Huang P, Yang R (2004) Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J Bacteriol 186(15):5147–5152. https://doi.org/10.1128/JB.186.15.5147-5152.2004
Zhang Y, Gao H, Wang L, Xiao X, Tan Y, Guo Z, Zhou D, Yang R (2011) Molecular characterization of transcriptional regulation of rovA by PhoP and RovA in Yersinia pestis. PLoS One 6(9):e25484. https://doi.org/10.1371/journal.pone.0025484
Liu L, Fang H, Yang H, Zhang Y, Han Y, Zhou D, Yang R (2016) CRP is an activator of Yersinia pestis biofilm formation that operates via a mechanism involving gmhA and waaAE-coaD. Front Microbiol 7:295. https://doi.org/10.3389/fmicb.2016.00295
El-Robh MS, Busby SJ (2002) The Escherichia coli cAMP receptor protein bound at a single target can activate transcription initiation at divergent promoters: a systematic study that exploits new promoter probe plasmids. Biochem J 368(Pt 3):835–843. https://doi.org/10.1042/BJ20021003
Zhou D, Yang R (2006) Global analysis of gene transcription regulation in prokaryotes. Cell Mol Life Sci 63(19–20):2260–2290. https://doi.org/10.1007/s00018-006-6184-6
Zhang Y (2018) Genetic regulation analysis of Yersinia pestis. In: Yang R (ed) Yersinia Pestis protocols springer protocols handbooks. Springer, Singapore. https://doi.org/10.1007/978-981-10-7947-4_22
Zhang Y, Wang L, Fang N, Qu S, Tan Y, Guo Z, Qiu J, Zhou D, Yang R (2013) Reciprocal regulation of pH 6 antigen gene loci by PhoP and RovA in Yersinia pestis biovar Microtus. Future Microbiol 8(2):271–280. https://doi.org/10.2217/fmb.12.146
Tam C, Demke O, Hermanas T, Mitchell A, Hendrickx AP, Schneewind O (2014) YfbA, a Yersinia pestis regulator required for colonization and biofilm formation in the gut of cat fleas. J Bacteriol 196(6):1165–1173. https://doi.org/10.1128/JB.01187-13
Fang H, Liu L, Zhang Y, Yang H, Yan Y, Ding X, Han Y, Zhou D, Yang R (2018) BfvR, an AraC-family regulator, controls biofilm formation and pH6 antigen production in opposite ways in Yersinia pestis Biovar Microtus. Front Cell Infect Microbiol 8:347. https://doi.org/10.3389/fcimb.2018.00347
Liu L, Fang N, Sun Y, Yang H, Zhang Y, Han Y, Zhou D, Yang R (2014) Transcriptional regulation of the waaAE-coaD operon by PhoP and RcsAB in Yersinia pestis biovar Microtus. Protein Cell 5(12):940–944. https://doi.org/10.1007/s13238-014-0110-8
Bontemps-Gallo S, Fernandez M, Dewitte A, Raphael E, Gherardini FC, Elizabeth P, Koch L, Biot F, Reboul A, Sebbane F (2019) Nutrient depletion may trigger the Yersinia pestis OmpR-EnvZ regulatory system to promote flea-borne plague transmission. Mol Microbiol 112(5):1471–1482. https://doi.org/10.1111/mmi.14372
Sun F, Gao H, Zhang Y, Wang L, Fang N, Tan Y, Guo Z, Xia P, Zhou D, Yang R (2012) Fur is a repressor of biofilm formation in Yersinia pestis. PLoS One 7(12):e52392. https://doi.org/10.1371/journal.pone.0052392
Silva-Rohwer AR, Held K, Sagawa J, Fernandez NL, Waters CM, Vadyvaloo V (2021) CsrA enhances cyclic-di-GMP biosynthesis and Yersinia pestis biofilm blockage of the flea foregut by alleviating Hfq-dependent repression of the hmsT mRNA. mbio. 12(4):e0135821. https://doi.org/10.1128/mBio.01358-21
Rempe KA, Hinz AK, Vadyvaloo V (2012) Hfq regulates biofilm gut blockage that facilitates flea-borne transmission of Yersinia pestis. J Bacteriol 194(8):2036–2040. https://doi.org/10.1128/JB.06568-11
Ni B, Wu HS, Xin YQ, Zhang QW, Zhang YQ (2021) Reciprocal regulation between Fur and two RyhB homologs in Yersinia pestis, and roles of RyhBs in biofilm formation. Biomed Environ Sci 34(4):299–308. https://doi.org/10.3967/bes2021.039
Liu Z, Gao X, Wang H, Fang H, Yan Y, Liu L, Chen R, Zhou D, Yang R, Han Y (2016) Plasmid pPCP1-derived sRNA HmsA promotes biofilm formation of Yersinia pestis. BMC Microbiol 16(1):176. https://doi.org/10.1186/s12866-016-0793-5
Zhang Y, Wang L, Han Y, Yan Y, Tan Y, Zhou L, Cui Y, Du Z, Wang X, Bi Y, Yang H, Song Y, Zhang P, Zhou D, Yang R (2013) Autoregulation of PhoP/PhoQ and positive regulation of the cyclic AMP receptor protein-cyclic AMP complex by PhoP in Yersinia pestis. J Bacteriol 195(5):1022–1030. https://doi.org/10.1128/JB.01530-12
Zhang Y, Sun F, Yang H, Liu L, Ni B, Huang X, Yang R, Zhou D (2015) CRP acts as a transcriptional repressor of the YPO1635-phoPQ-YPO1632 operon in Yersinia pestis. Curr Microbiol 70(3):398–403. https://doi.org/10.1007/s00284-014-0736-z
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This work was supported by the Basic Application Research Project of Science and Technology Department of Qinghai province (2020-ZJ-788), the National Natural Science Foundation of China (81801984) and the China Postdoctoral Science Foundation (2019M664008).
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YZ and QZ: designed, organized and supervised the experiments, interpreted the results, and edited the manuscript. LL, WL, YH, YL and HW: performed the laboratory experiments. LL and YZ: drafted the manuscript.
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Liu, L., Liu, W., He, Y. et al. Transcriptional Regulation of hmsB, A Temperature-Dependent Small RNA, by RovM in Yersinia pestis Biovar Microtus. Curr Microbiol 80, 182 (2023). https://doi.org/10.1007/s00284-023-03293-1
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DOI: https://doi.org/10.1007/s00284-023-03293-1