沙门菌非编码小RNA RyhB研究进展

doi:10.11843/j.issn.0366-6964.2019.01.003

Abstract

Abstract:

Small non-coding RNA (sRNA) is a type of RNA molecule that is transcribed but not translated into protein in the genome and controls gene expression at the post-transcriptional level. Unlike protein-mediated regulation system, sRNA-mediated regulation can respond to environmental changes quickly when bacteria confront adverse growth environment. RyhB-1 and RyhB-2 are two highly homologous sRNAs in Salmonella, which regulate target genes expression singly or together with the help of regulating factors by base pairing. RyhB-1 and RyhB-2 are major components of Salmonella iron homeostasis regulation at post-transcriptional level by increasing the iron uptake, limiting non-essential iron-utilizing proteins synthesis and accelerating the storage of iron-sulfur protein when iron is scarce. In addition, when Salmonella encounters various environmental stresses such as oxidative stress, hypoxia or acidic environment, RyhB can also control the production of reactive oxygen species, balance the stability of inorganic substances such as nitrate, and regulate bacterial motility and Salmonella virulence to cope with environmental changes. This paper is concerned with the physiological characteristics, regulatory mechanisms and functions of Salmonella RyhB to provide guidance for the subsequent study of RyhB.

Key words: small non-coding RNA, Salmonella, RyhB

CLC Number:

S852.612

CHEN Binjie, WANG Heng, CHEN Yanfei, PAN Xiayu, YUAN Tianmei, ZHU Guoqiang, MENG Xia. Research Progress on Small Non-Coding RNA RyhB of Salmonella[J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(1): 21-27.

References

[1] 陆承平. 兽医微生物学[M]. 5版. 北京:中国农业出版社, 2013.
LU C P. Veterinary microbiology[M]. 5th ed. Beijing:China Agriculture Press, 2013. (in Chinese)
[2] QUEREDA J J, COSSART P. Regulating bacterial virulence with RNA[J]. Annu Rev Microbiol, 2017, 71:263-280.
[3] PAPENFORT K, VOGEL J. Regulatory RNA in bacterial pathogens[J]. Cell Host Microbe, 2010, 8(1):116-127.
[4] ZHANG S S, LIU S, WU N, et al. Small non-coding RNA RyhB mediates persistence to multiple antibiotics and stresses in uropathogenic Escherichia coli by reducing cellular metabolism[J]. Front Microbiol, 2018, 9:136.
[5] STORZ G, VOGEL J, WASSARMAN K M. Regulation by small RNAs in bacteria:expanding frontiers[J]. Mol Cell, 2011, 43(6):880-891.
[6] 孟霞,王亨,朱国强. 沙门菌非编码小RNA调控功能研究进展[J]. 中国兽医学报, 2011, 31(12):1803-1808.
MENG X, WANG H, ZHU G Q. Regulation function of non-coding small RNA in Salmonella[J]. Chinese Journal of Veterinary Science, 2011, 31(12):1803-1808. (in Chinese)
[7] VECEREK B, MOLL I, BLÄSI U. Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding[J]. EMBO J, 2007, 26(4):965-975.
[8] PORCHERON G, DOZOIS C M. Interplay between iron homeostasis and virulence:Fur and RyhB as major regulators of bacterial pathogenicity[J]. Vet Microbiol, 2015, 179(1-2):2-14.
[9] MASSÉ E, VANDERPOOL C K, GOTTESMAN S. Effect of RyhB small RNA on global iron use in Escherichia coli[J]. J Bacteriol, 2005, 187(20):6962-6971.
[10] MANDIN P, CHAREYRE S, BARRAS F. A Regulatory circuit composed of a transcription factor, IscR, and a regulatory RNA, RyhB, controls Fe-S cluster delivery[J]. mBio, 2016, 7(5):e00966-16.
[11] BOS J, DUVERGER Y, THOUVENOT B, et al. The sRNA RyhB regulates the synthesis of the Escherichia coli methionine sulfoxide reductase MsrB but not MsrA[J]. PLoS One, 2013, 8(5):e63647.
[12] ARGAMAN L, HERSHBERG R, VOGEL J, et al. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli[J]. Curr Biol, 2001, 11(12):941-950.
[13] MASSÉ E, GOTTESMAN S. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli[J]. Proc Natl Acad Sci U S A, 2002, 99(7):4620-4625.
[14] LECLERC J M, DOZOIS C M, DAIGLE F. Role of the Salmonella enterica serovar Typhi Fur regulator and small RNAs RfrA and RfrB in iron homeostasis and interaction with host cells[J]. Microbiology, 2013, 159:591-602.
[15] ELLERMEIER J R, SLAUCH J M. Fur regulates expression of the Salmonella pathogenicity island 1 type Ⅲ secretion system through HilD[J]. J Bacteriol, 2008, 190(2):476-486.
[16] KIM J N, KWON Y M. Genetic and phenotypic characterization of the RyhB regulon in Salmonella Typhimurium[J]. Microbiol Res, 2013, 168(1):41-49.
[17] SINHA D, MATZ L, CAMERON T, et al. Poly(A) polymerase is required for RyhB sRNA stability and function in Escherichia coli[J]. RNA, 2018, 24(11):1496-1511.
[18] CHAREYRE S, MANDIN P. Bacterial iron homeostasis regulation by sRNAs[J]. Microbiol Spectr, 2018, 6(2), doi:10.1128/microbiolspec. RWR-0010-2017.
[19] CALDERÓN I L, MORALES E H, COLLAO B, et al. Role of Salmonella typhimurium small RNAs RyhB-1 and RyhB-2 in the oxidative stress response[J]. Res Microbiol, 2014, 165(1):30-40.
[20] NEGRETE A, SHILOACH J. Improving E. coli growth performance by manipulating small RNA expression[J]. Microb Cell Fact, 2017, 16:198.
[21] TEIXIDÓ L, CORTÉS P, BIGAS A, et al. Control by Fur of the nitrate respiration regulators NarP and NarL in Salmonella enterica[J]. Int Microbiol, 2010, 13(1):33-39.
[22] CALDERÓN P F, MORALES E H, ACUÑA L G, et al. The small RNA RyhB homologs from Salmonella typhimurium participate in the response to S-nitrosoglutathione-induced stress[J]. Biochem Biophys Res Commun, 2014, 450(1):641-645.
[23] KIM J N, KWON Y M. Identification of target transcripts regulated by small RNA RyhB homologs in Salmonella:RyhB-2 regulates motility phenotype[J]. Microbiol Res, 2013, 168(10):621-629.
[24] KIM J N, KWON Y M. Phenotypic characterization of Salmonella RyhB-1 mutations that modulate target regulation[J]. Curr Microbiol, 2014, 69(2):212-217.
[25] PADALON-BRAUCH G, HERSHBERG R, ELGRABLY-WEISS M, et al. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence[J]. Nucleic Acids Res, 2008, 36(6):1913-1927.
[26] THODE S K, BAEKKEDAL C, SÖDERBERG J J, et al. Construction of a fur null mutant and RNA-sequencing provide deeper global understanding of the Aliivibrio salmonicida Fur regulon[J]. PeerJ, 2017, 5:e3461.
[27] BAICHOO N, HELMANN J D. Recognition of DNA by Fur:a reinterpretation of the Fur box consensus sequence[J]. J Bacteriol, 2002, 184(21):5826-5832.
[28] GEISSMANN T A, TOUATI D. Hfq, a new chaperoning role:binding to messenger RNA determines access for small RNA regulator[J]. EMBO J, 2004, 23(2):396-405.
[29] MORITA T, NISHINO R, AIBA H. Role of the terminator hairpin in the biogenesis of functional Hfq-binding sRNAs[J]. RNA, 2017, 23(9):1419-1431.
[30] SCHU D J, ZHANG A X, GOTTESMAN S, et al. Alternative Hfq-sRNA interaction modes dictate alternative mRNA recognition[J]. EMBO J, 2015, 34(20):2557-2573.
[31] MORITA T, UEDA M, KUBO K, et al. Insights into transcription termination of Hfq-binding sRNAs of Escherichia coli and characterization of readthrough products[J]. RNA, 2015, 21(8):1490-1501.
[32] MELAMED S, PEER A, FAIGENBAUM-ROMM R, et al. Global mapping of small RNA-target interactions in bacteria[J]. Mol Cell, 2016, 63(5):884-897.
[33] ARBEL-GOREN R, TAL A, PARASAR B, et al. Transcript degradation and noise of small RNA-controlled genes in a switch activated network in Escherichia coli[J]. Nucleic Acids Res, 2016, 44(14):6707-6720.
[34] MORITA T, AIBA H. RNase E action at a distance:degradation of target mRNAs mediated by an Hfq-binding small RNA in bacteria[J]. Genes Dev, 2011, 25(4):294-298.
[35] MACKIE G A. RNase E:at the interface of bacterial RNA processing and decay[J]. Nat Rev Microbiol, 2013, 11(1):45-57.
[36] AFONYUSHKIN T, VECEREK B, MOLL I, et al. Both RNase E and RNase Ⅲ control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB[J]. Nucleic Acids Res, 2005, 33(5):1678-1689.
[37] BRIANI F, CARZANIGA T, DEHÒ G. Regulation and functions of bacterial PNPase[J]. Wiley Interdiscip Rev RNA, 2016, 7(2):241-258.
[38] DENG Z L, LIU Z Z, BI Y J, et al. Rapid degradation of Hfq-free RyhB in Yersinia pestis by PNPase independent of putative ribonucleolytic complexes[J]. BioMed Res Int, 2014, 2014:798918.
[39] MORITA T, MAKI K, AIBA H. RNase E-based ribonucleoprotein complexes:mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs[J]. Genes Dev, 2005, 19(18):2176-2186.
[40] MORITA T, MOCHIZUKI Y, AIBA H. Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction[J]. Proc Natl Acad Sci U S A, 2006, 103(13):4858-4863.
[41] WOOLDRIDGE K G, WILLIAMS P H. Iron uptake mechanisms of pathogenic bacteria[J]. FEMS Microbiol Rev, 1993, 12(4):325-348.
[42] ANDREWS S C, ROBINSON A K, RODRÍGUEZ-QUIÑONES F. Bacterial iron homeostasis[J]. FEMS Microbiol Rev, 2003, 27(2-3):215-237.
[43] MASSÉ E, SALVAIL H, DESNOYERS G, et al. Small RNAs controlling iron metabolism[J]. Curr Opin Microbiol, 2007, 10(2):140-145.
[44] SEMSEY S, ANDERSSON A M C, KRISHNA S, et al. Genetic regulation of fluxes:iron homeostasis of Escherichia coli[J]. Nucleic Acids Res, 2006, 34(17):4960-4967.
[45] SALVAIL H, LANTHIER-BOURBONNAIS P, SOBOTA J M, et al. A small RNA promotes siderophore production through transcriptional and metabolic remodeling[J]. Proc Natl Acad Sci U S A, 2010, 107(34):15223-15228.
[46] CHU B C, GARCIA-HERRERO A, JOHANSON T H, et al. Siderophore uptake in bacteria and the battle for iron with the host;a bird's eye view[J]. Biometals, 2010, 23(4):601-611.
[47] TRONNET S, GARCIE C, REHM N, et al. Iron homeostasis regulates the genotoxicity of Escherichia coli that produces colibactin[J]. Infect Immun, 2016, 84(12):3358-3368.
[48] NANDAL A, HUGGINS C C O, WOODHALL M R, et al. Induction of the ferritin gene (ftnA) of Escherichia coli by Fe²⁺-Fur is mediated by reversal of H-NS silencing and is RyhB independent[J]. Mol Microbiol, 2010, 75(3):637-657.
[49] BAEZ A, SHILOACH J. Increasing dissolved-oxygen disrupts iron homeostasis in production cultures of Escherichia coli[J]. Antonie Van Leeuwenhoek, 2017, 110(1):115-124.
[50] TRONNET S, GARCIE C, BRACHMANN A O, et al. High iron supply inhibits the synthesis of the genotoxin colibactin by pathogenic Escherichia coli through a non-canonical Fur/RyhB-mediated pathway[J]. Pathog Dis, 2017, 75(5), doi:10.1093/femspd/ftx066.
[51] JACQUES J F, JANG S, PRÉVOST K, et al. RyhB small RNA modulates the free intracellular iron pool and is essential for normal growth during iron limitation in Escherichia coli[J]. Mol Microbiol, 2006, 62(4):1181-1190.
[52] MAILLOUX R J, LEMIRE J, APPANNA V D. Metabolic networks to combat oxidative stress in Pseudomonas fluorescens[J]. Antonie Van Leeuwenhoek, 2011, 99(3):433-442.
[53] WU Y, HAO Y Q, WEI X, et al. Impairment of NADH dehydrogenase and regulation of anaerobic metabolism by the small RNA RyhB and NadE for improved biohydrogen production in Enterobacter aerogenes[J]. Biotechnol Biofuels, 2017, 10:248.
[54] OGLESBY A G, MURPHY E R, IYER V R, et al. Fur regulates acid resistance in Shigella flexneri via RyhB and ydeP[J]. Mol Microbiol, 2005, 58(5):1354-1367.
[55] STEWART V, PARALES Jr J. Identification and expression of genes narL and narX of the nar (nitrate reductase) locus in Escherichia coli K-12[J]. J Bacteriol, 1988, 170(4):1589-1597.
[56] GUNSALUS R P. Control of electron flow in Escherichia coli:coordinated transcription of respiratory pathway genes[J]. J Bacteriol, 1992, 174(22):7069-7074.
[57] 倪杰. 非编码小RNA RyhB-1与IsrE在肠炎沙门氏菌致病性上的相互作用研究[D]. 扬州:扬州大学, 2016.
NI J. Interaction of small non-coding RNA RyhB-1 and IsrE in the pathogenicity of Salmonella enteritidis[D]. Yangzhou:Yangzhou University, 2016. (in Chinese)
[58] 张彬彬,羊扬,刘云,等. Ⅰ型群体感应系统对禽致病性大肠杆菌生物被膜形成的调控机制研究[J]. 中国家禽, 2015, 37(24):19-23.
ZHANG B B, YANG Y, LIU Y, et al. Study on regulatory mechanism of quorum sensing Ⅰ on biofilm in avian pathogenic Escherichia coli[J]. China Poultry, 2015, 37(24):19-23. (in Chinese)
[59] MEY A R, CRAIG S A, PAYNE S M. Characterization of Vibrio cholerae RyhB:the RyhB regulon and role of ryhB in biofilm formation[J]. Infect Immun, 2005, 73(9):5706-5719.
[60] 倪杰,孟宪臣,李芙蓉,等. 肠炎沙门菌非编码小RNA RyhB-1和IsrE对清远麻鸡的致病性[J]. 中国兽医学报, 2017, 37(9):1687-1692.
NI J, MENG X C, LI F R, et al. Pathogenicity of Salmonella enteritidis non-coding small RNAs RyhB-1 and IsrE in Qingyuan chickens[J]. Chinese Journal of Veterinary Science, 2017, 37(9):1687-1692. (in Chinese)

Research Progress on Small Non-Coding RNA RyhB of Salmonella

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	LIU Lijuan, DONG Ranran, WANG Kaigong, CHENG Zhentao, WEN Ming, WEN Guilan, LI Chen, YANG Qi, ZHOU Bijun. mRNA-Seq Whole-transcriptome Analysis of sRNA gcvB Deletion Background in Salmonella [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(4): 840-850.
[2]	LIU Lijuan, DONG Ranran, WANG Kaigong, CHENG Zhentao, WEN Ming, WEN Guilan, LI Chen, YANG Qi, ZHOU Bijun. mRNA-Seq Whole-transcriptome Analysis of sRNA gcvB Deletion Background in Salmonella [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(4): 840-850.
[3]	ZHANG Jin, LI Qinghe, ZHENG Maiqing, LIU Ranran, CUI Huanxian, WEN Jie, ZHAO Guiping. Analysis of Regulatory T Cells Changes in Chicks Infected with Salmonella [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(11): 2302-2308.
[4]	CHEN Binjie, WANG Heng, CHEN Yanfei, PAN Xiayu, YUAN Tianmei, ZHU Guoqiang, MENG Xia. Research Progress on Small Non-Coding RNA RyhB of Salmonella [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2019, 50(1): 21-27.
[5]	XU Yao-hui, DENG Tong-wei, QI Ya-ru, HAN Wen-long, LU Jian-zhou, JIANG Zeng-hai. Isolation, Identification and Antimicrobial Resistance of Salmonella from Dead Chicken Embryos in Sanhuang Breeder Farms [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(5): 1081-1088.
[6]	XU Yao-hui, DENG Tong-wei, QI Ya-ru, HAN Wen-long, LU Jian-zhou, JIANG Zeng-hai. Isolation, Identification and Antimicrobial Resistance of Salmonella from Dead Chicken Embryos in Sanhuang Breeder Farms [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(5): 1081-1088.
[7]	CHEN Tong, ZHU Yu-xing, CAI Wen-yi, YANG Qi-yue, DENG Zhi-he, LAN Dao-liang. Screening of Differentially Expressed Genes Associated with Salmonella Infection from Spleen of Artificially Infected Yak [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(4): 794-803.
[8]	CHEN Tong, ZHU Yu-xing, CAI Wen-yi, YANG Qi-yue, DENG Zhi-he, LAN Dao-liang. Screening of Differentially Expressed Genes Associated with Salmonella Infection from Spleen of Artificially Infected Yak [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(4): 794-803.
[9]	WANG Yan-qiu, WU Li-yun, CHEN Xiao-gang, SUN Tong, LI Chong, YU Dao-jin. Establishment and Optimization of the Acid Tolerance Response Model for Salmonella Enteritidis [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(2): 401-411.
[10]	WANG Yan-qiu, WU Li-yun, CHEN Xiao-gang, SUN Tong, LI Chong, YU Dao-jin. Establishment and Optimization of the Acid Tolerance Response Model for Salmonella Enteritidis [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2018, 49(2): 401-411.
[11]	XIA Bin-yan, WANG Jing-jing, TANG Cheng, TAN Shuo, FENG Fan, CHEN Ji-kui, YUE Hua. Distribution of Serovars and Virulence Genes in Salmonella Isolates from Goats in Sichuan Province [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2017, 48(11): 2157-2165.
[12]	XIA Bin-yan, WANG Jing-jing, TANG Cheng, TAN Shuo, FENG Fan, CHEN Ji-kui, YUE Hua. Distribution of Serovars and Virulence Genes in Salmonella Isolates from Goats in Sichuan Province [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2017, 48(11): 2157-2165.
[13]	YIN Lei，QI Ke-zong，TU Jian，ZHOU Xiu-hong，LIU Hong-mei，WANG Man，ZHANG Yan-na. Analysis of the Regulation of Small Non-coding RNA (RyhB) on Avian Pathogenic Escherichia coli Virulence-related Genes [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2015, 46(8): 1409-1416.
[14]	YIN Lei，QI Ke-zong，TU Jian，ZHOU Xiu-hong，LIU Hong-mei，WANG Man，ZHANG Yan-na. Analysis of the Regulation of Small Non-coding RNA (RyhB) on Avian Pathogenic Escherichia coli Virulence-related Genes [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2015, 46(8): 1409-1416.
[15]	GENG Shi-zhong，CHEN Xiao-juan，PAN Zhi-ming，JIAO Xin-an. Construction and Preliminary Application of Balanced Lethal System Based on Attenuated Salmonella SG97A [J]. ACTA VETERINARIA ET ZOOTECHNICA SINICA, 2015, 46(12): 2243-2250.