Transcriptomic dissection of the horizontally acquired response regulator EsrB reveals its global regulatory roles in the physiological adaptation and activation of T3SS and the cognate effector repertoire in Edwardsiella piscicida during infection toward turbot

References

• Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annu Rev Biochem 2000; 69:183-215; PMID:10966457; https://doi.org/10.1146/annurev.biochem.69.1.183
   PubMed Web of Science ®Google Scholar
• Mitrophanov AY, Groisman EA. Signal integration in bacterial two-component regulatory systems. Genes Dev 2008; 22(19):2601-11; PMID:18832064; https://doi.org/10.1101/gad.1700308
   PubMed Web of Science ®Google Scholar
• Li L, Wang Q, Zhang H, Yang M, Khan MI, Zhou X. Sensor histidine kinase is a beta-lactam receptor and induces resistance to beta-lactam antibiotics. Proc Natl Acad Sci U S A 2016; 113(6):1648-53; PMID:26831117; https://doi.org/10.1073/pnas.1520300113
   PubMed Web of Science ®Google Scholar
• Rasko DA, Moreira CG, Li DR, Reading NC, Ritchie JM, Waldor MK, Williams N, Taussig R, Wei S, Roth M. Targeting QseC signaling and virulence for antibiotic development. Science 2008; 321(5892):1078-80; PMID:18719281; https://doi.org/10.1126/science.1160354
   PubMed Web of Science ®Google Scholar
• Wang Q, Yang M, Xiao J, Wu H, Wang X, Lv Y, Xu L, Zheng H, Wang S, Zhao G. Genome sequence of the versatile fish pathogen Edwardsiella tarda provides insights into its adaptation to broad host ranges and intracellular niches. PLoS One 2009; 4(10):e7646; PMID:19865481; https://doi.org/10.1371/journal.pone.0007646
   PubMed Web of Science ®Google Scholar
• Yang M, Lv Y, Xiao J, Wu H, Zheng H, Liu Q, Zhang Y, Wang Q. Edwardsiella comparative phylogenomics reveal the new intra/inter-species taxonomic relationships, virulence evolution and niche adaptation mechanisms. PLoS One 2012; 7(5):e36987; PMID:22590641; https://doi.org/10.1371/journal.pone.0036987
   PubMed Web of Science ®Google Scholar
• Abayneh T, Colquhoun DJ, Sorum H. Edwardsiella piscicida sp. nov., a novel species pathogenic to fish. J Appl Microbiol 2013; 114(3):644-54; PMID:23167785; https://doi.org/10.1111/jam.12080
   PubMed Web of Science ®Google Scholar
• Shao S, Lai Q, Liu Q, Wu H, Xiao J, Shao Z, Wang Q, Zhang Y. Phylogenomics characterization of a highly virulent Edwardsiella strain ET080813(T) encoding two distinct T3SS and three T6SS gene clusters: Propose a novel species as Edwardsiella anguillarum sp. nov. Syst Appl Microbiol 2015; 38(1):36-47; PMID:25466920; https://doi.org/10.1016/j.syapm.2014.10.008
   PubMed Web of Science ®Google Scholar
• Janda JM, Abbott SL. Infections associated with the genus Edwardsiella: the role of Edwardsiella tarda in human disease. Clin Infect Dis 1993; 17(4):742-8; PMID:8268359; https://doi.org/10.1093/clinids/17.4.742
   PubMed Web of Science ®Google Scholar
• Thune RL, Stanley LA, Cooper RK. Pathogenesis of gram-negative bacterial infections in warmwater fish. Ann Rev Fish Dis 1993; 3:37-68; https://doi.org/10.1016/0959-8030(93)90028-A
   Google Scholar
• Leung KY, Siame BA, Tenkink BJ, Noort RJ, Mok YK. Edwardsiella tarda - virulence mechanisms of an emerging gastroenteritis pathogen. Microbes Infect 2012; 14(1):26-34; PMID:21924375; https://doi.org/10.1016/j.micinf.2011.08.005
   PubMed Web of Science ®Google Scholar
• Park SB, Aoki T, Jung TS. Pathogenesis of and strategies for preventing Edwardsiella tarda infection in fish. Vet Res 2012; 43(1):67; PMID:23035843; https://doi.org/10.1186/1297-9716-43-67
   PubMed Web of Science ®Google Scholar
• Sakai T, Kanai K, Osatomi K, Yoshikoshi K. Identification of a 19.3-kDa protein in MRHA-positive Edwardsiella tarda: putative fimbrial major subunit. FEMS Microbiol Lett 2003; 226(1):127-33; PMID:13129618; https://doi.org/10.1016/S0378-1097(03)00608-6
   PubMed Web of Science ®Google Scholar
• Sakai T, Matsuyama T, Sano M, Iida T. Identification of novel putative virulence factors, adhesin AIDA and type VI secretion system, in atypical strains of fish pathogenic Edwardsiella tarda by genomic subtractive hybridization. Microbiol Immunol 2009; 53(3):131-9; PMID:19302523; https://doi.org/10.1111/j.1348-0421.2009.00108.x
   PubMed Web of Science ®Google Scholar
• Hu YH, Sun L. The global regulatory effect of Edwardsiella tarda Fur on iron acquisition, stress resistance, and host infection: A proteomics-based interpretation. J Proteomics 2016; 140:100-10; PMID:27102497; https://doi.org/10.1016/j.jprot.2016.04.005
   PubMed Web of Science ®Google Scholar
• Wang X, Wang Q, Xiao J, Liu Q, Wu H, Zhang Y. Hemolysin EthA in Edwardsiella tarda is essential for fish invasion in vivo and in vitro and regulated by two-component system EsrA-EsrB and nucleoid protein HhaEt. Fish Shellfish Immunol 2010; 29(6):1082-91; PMID:20832475; https://doi.org/10.1016/j.fsi.2010.08.025
   PubMed Web of Science ®Google Scholar
• Srinivasa RP, Lim TM, Leung KY. Functional genomics approach to the identification of virulence genes involved in Edwardsiella tarda pathogenesis. Infect Immun 2003; 71(3):1343-51; PMID:12595451; https://doi.org/10.1128/IAI.71.3.1343-1351.2003
   PubMed Web of Science ®Google Scholar
• Wang X, Wang Q, Xiao J, Liu Q, Wu H, Xu L, Zhang Y. Edwardsiella tarda T6SS component evpP is regulated by esrB and iron, and plays essential roles in the invasion of fish. Fish Shellfish Immunol 2009; 27(3):469-77; PMID:19563898; https://doi.org/10.1016/j.fsi.2009.06.013
   PubMed Web of Science ®Google Scholar
• Jiao XD, Zhang M, Cheng S, Sun L. Analysis of Edwardsiella tarda DegP, a serine protease and a protective immunogen. Fish Shellfish Immunol 2010; 28(4):672-7; PMID:20060910; https://doi.org/10.1016/j.fsi.2010.01.004
   PubMed Web of Science ®Google Scholar
• Lv Y, Yin K, Shao S, Wang Q, Zhang Y. Comparative proteomic analysis reveals new components of the PhoP regulon and highlights a role for PhoP in the regulation of genes encoding the F1F0 ATP synthase in Edwardsiella tarda. Microbiology 2013; 159(7):1340-51; PMID:23657683; https://doi.org/10.1099/mic.0.066803-0
   PubMed Web of Science ®Google Scholar
• Zhou ZJ, Sun BG, Sun L. Edwardsiella tarda Sip1: A serum-induced zinc metalloprotease that is essential to serum resistance and host infection. Vet Microbiol 2015; 177(3-4):332-40; PMID:25899393; https://doi.org/10.1016/j.vetmic.2015.03.030
   PubMed Web of Science ®Google Scholar
• Tan YP, Zheng J, Tung SL, Rosenshine I, Leung KY. Role of type III secretion in Edwardsiella tarda virulence. Microbiology 2005; 151(7):2301-13; PMID:16000720; https://doi.org/10.1099/mic.0.28005-0
   PubMed Web of Science ®Google Scholar
• Okuda J, Kiriyama M, Suzaki E, Kataoka K, Nishibuchi M, Nakai T. Characterization of proteins secreted from a type III secretion system of Edwardsiella tarda and their roles in macrophage infection. Dis Aquat Organ 2009; 84(2):115-21; PMID:19476281; https://doi.org/10.3354/dao02033
   PubMed Web of Science ®Google Scholar
• Hou M, Chen R, Yang D, Nunez G, Wang Z, Wang Q, Zhang Y, Liu Q. Identification and functional characterization of EseH, a new effector of the type III secretion system of Edwardsiella piscicida. Cell Microbiol 2017;19(1): e12638; https://doi.org/10.1111/cmi.12638
   Web of Science ®Google Scholar
• Strauss EJ, Ghori N, Falkow S. An Edwardsiella tarda strain containing a mutation in a gene with homology to shlB and hpmB is defective for entry into epithelial cells in culture. Infect Immun 1997; 65(9):3924-32; PMID:9284172
   PubMed Web of Science ®Google Scholar
• Zheng J, Leung KY. Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 2007; 66(5):1192-206; PMID:17986187; https://doi.org/10.1111/j.1365-2958.2007.05993.x
   PubMed Web of Science ®Google Scholar
• Xie HX, Lu JF, Rolhion N, Holden DW, Nie P, Zhou Y, Yu XJ. Edwardsiella tarda-induced cytotoxicity depends on its type III secretion system and flagellin. Infect Immun 2014; 82(8):3436-45; PMID:24891103; https://doi.org/10.1128/IAI.01065-13
   PubMed Web of Science ®Google Scholar
• Fang S, Zhang L, Lou Y, Yang D, Wang Q, Zhang Y, Liu Q. Intracellular translocation and localization of Edwardsiella tarda type III secretion system effector EseG in host cells. Microb Pathog 2016; 97:166-71; PMID:27208750; https://doi.org/10.1016/j.micpath.2016.05.008
   PubMed Web of Science ®Google Scholar
• Xie HX, Yu HB, Zheng J, Nie P, Foster LJ, Mok YK, Finlay BB, Leung KY. EseG, an effector of the type III secretion system of Edwardsiella tarda, triggers microtubule destabilization. Infect Immun 2010; 78(12):5011-21; PMID:20855515; https://doi.org/10.1128/IAI.00152-10
   PubMed Web of Science ®Google Scholar
• Xie HX, Lu JF, Zhou Y, Yi J, Yu XJ, Leung KY, Nie P. Identification and functional characterization of the novel Edwardsiella tarda effector EseJ. Infect Immun 2015; 83(4):1650-60; PMID:25667268; https://doi.org/10.1128/IAI.02566-14
   PubMed Web of Science ®Google Scholar
• Lv Y, Xiao J, Liu Q, Wu H, Zhang Y, Wang Q. Systematic mutation analysis of two-component signal transduction systems reveals EsrA-EsrB and PhoP-PhoQ as the major virulence regulators in Edwardsiella tarda. Vet Microbiol 2012; 157(1-2):190-9; PMID:22227416; https://doi.org/10.1016/j.vetmic.2011.12.018
   PubMed Web of Science ®Google Scholar
• Brown NF, Rogers LD, Sanderson KL, Gouw JW, Hartland EL, Foster LJ. A horizontally acquired transcription factor coordinates Salmonella adaptations to host microenvironments. mBio 2014; 5(5):e1714-27; https://doi.org/10.1128/mBio.01727-14
   Web of Science ®Google Scholar
• Tomljenovic-Berube AM, Mulder DT, Whiteside MD, Brinkman FS, Coombes BK. Identification of the regulatory logic controlling Salmonella pathoadaptation by the SsrA-SsrB two-component system. PLoS Genet 2010; 6(3):e1000875; PMID:20300643; https://doi.org/10.1371/journal.pgen.1000875
   PubMed Web of Science ®Google Scholar
• Desai SK, Winardhi RS, Periasamy S, Dykas MM, Jie Y, Kenney LJ. The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing. Elife 2016; 5: e10747; PMID:26880544; https://doi.org/10.7554/eLife.10747
   PubMed Web of Science ®Google Scholar
• Rogge ML, Thune RL. Regulation of the Edwardsiella ictaluri type III secretion system by pH and phosphate concentration through EsrA, EsrB, and EsrC. Appl Environ Microbiol 2011; 77(13):4293-302; PMID:21551284; https://doi.org/10.1128/AEM.00195-11
   PubMed Web of Science ®Google Scholar
• Zheng J, Tung SL, Leung KY. Regulation of a type III and a putative secretion system in Edwardsiella tarda by EsrC is under the control of a two-component system, EsrA-EsrB. Infect Immun 2005; 73(7):4127-37; PMID:15972502; https://doi.org/10.1128/IAI.73.7.4127-4137.2005
   PubMed Web of Science ®Google Scholar
• Chakraborty S, Sivaraman J, Leung KY, Mok YK. Two-component PhoB-PhoR regulatory system and ferric uptake regulator sense phosphate and iron to control virulence genes in type III and VI secretion systems of Edwardsiella tarda. J Biol Chem 2011; 286(45):39417-30; PMID:21953460; https://doi.org/10.1074/jbc.M111.295188
   PubMed Web of Science ®Google Scholar
• Yang W, Wang L, Zhang L, Qu J, Wang Q, Zhang Y. An invasive and low virulent Edwardsiella tarda esrB mutant promising as live attenuated vaccine in aquaculture. Appl Microbiol Biotechnol 2015; 99(4):1765-77; PMID:25431010; https://doi.org/10.1007/s00253-014-6214-5
   PubMed Web of Science ®Google Scholar
• Lan MZ, Peng X, Xiang MY, Xia ZY, Bo W, Jie L, Li XY, Jun ZP. Construction and characterization of a live, attenuated esrB mutant of Edwardsiella tarda and its potential as a vaccine against the haemorrhagic septicaemia in turbot, Scophthamus maximus (L.). Fish Shellfish Immunol 2007; 23(3):521-30; PMID:17478097; https://doi.org/10.1016/j.fsi.2006.11.002
   PubMed Web of Science ®Google Scholar
• Gao ZP, Nie P, Lu JF, Liu LY, Xiao TY, Liu W, Liu JS, Xie HX. Type III secretion system translocon component EseB forms filaments on and mediates autoaggregation of and biofilm formation by Edwardsiella tarda. Appl Environ Microbiol 2015; 81(17):6078-87; PMID:26116669; https://doi.org/10.1128/AEM.01254-15
   PubMed Web of Science ®Google Scholar
• Rao PS, Yamada Y, Tan YP, Leung KY. Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol Microbiol 2004; 53(2):573-86; PMID:15228535; https://doi.org/10.1111/j.1365-2958.2004.04123.x
   PubMed Web of Science ®Google Scholar
• Nydam SD, Shah DH, Call DR. Transcriptome analysis of Vibrio parahaemolyticus in type III secretion system 1 inducing conditions. Front Cell Infect Microbiol 2014; 4:1; PMID:24478989; https://doi.org/10.3389/fcimb.2014.00001
   PubMed Web of Science ®Google Scholar
• Aguilera L, Ferreira E, Gimenez R, Fernandez FJ, Taules M, Aguilar J, Vega MC, Badia J, Baldoma L. Secretion of the housekeeping protein glyceraldehyde-3-phosphate dehydrogenase by the LEE-encoded type III secretion system in enteropathogenic Escherichia coli. Int J Biochem Cell Biol 2012; 44(6):955-62; PMID:22433988; https://doi.org/10.1016/j.biocel.2012.03.002
   PubMed Web of Science ®Google Scholar
• Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010; 11(10):R106; PMID:20979621; https://doi.org/10.1186/gb-2010-11-10-r106
   PubMed Web of Science ®Google Scholar
• Hirono I, Tange N, Aoki T. Iron-regulated haemolysin gene from Edwardsiella tarda. Mol Microbiol 1997; 24(4):851-6; PMID:9194711; https://doi.org/10.1046/j.1365-2958.1997.3971760.x
   PubMed Web of Science ®Google Scholar
• Santander J, Golden G, Wanda SY, Curtiss RR. Fur-regulated iron uptake system of Edwardsiella ictaluri and its influence on pathogenesis and immunogenicity in the catfish host. Infect Immun 2012; 80(8):2689-703; PMID:22615248; https://doi.org/10.1128/IAI.00013-12
   PubMed Web of Science ®Google Scholar
• Zhang L, Ni C, Xu W, Dai T, Yang D, Wang Q, Zhang Y, Liu Q. Intramacrophage infection reinforces the virulence of Edwardsiella tarda. J Bacteriol 2016; 198(10):1534-42; PMID:26953340; https://doi.org/10.1128/JB.00978-15
   PubMed Web of Science ®Google Scholar
• Charpentier X, Oswald E. Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 2004; 186(16):5486-95; PMID:15292151; https://doi.org/10.1128/JB.186.16.5486-5495.2004
   PubMed Web of Science ®Google Scholar
• Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 2013; 500(7462):350-3; PMID:23925114; https://doi.org/10.1038/nature12453
   PubMed Web of Science ®Google Scholar
• Wang X, Wang Q, Yang M, Xiao J, Liu Q, Wu H, Zhang Y. QseBC controls flagellar motility, fimbrial hemagglutination and intracellular virulence in fish pathogen Edwardsiella tarda. Fish Shellfish Immunol 2011; 30(3):944-53; PMID:21288493; https://doi.org/10.1016/j.fsi.2011.01.019
   PubMed Web of Science ®Google Scholar
• Yin K, Wang Q, Xiao J, Zhang Y. Comparative proteomic analysis unravels a role for EsrB in the regulation of reactive oxygen species stress responses in Edwardsiella piscicida. FEMS Microbiol Lett 2016; 364(1):fnw269; PMID:27915248; https://doi.org/10.1093/femsle/fnw269
   PubMed Web of Science ®Google Scholar
• Mota LJ, Cornelis GR. The bacterial injection kit: type III secretion systems. Ann Med 2005; 37(4):234-49; PMID:16019722; https://doi.org/10.1080/07853890510037329
   PubMed Web of Science ®Google Scholar
• Coburn B, Sekirov I, Finlay BB. Type III secretion systems and disease. Clin Microbiol Rev 2007; 20(4):535-49; PMID:17934073; https://doi.org/10.1128/CMR.00013-07
   PubMed Web of Science ®Google Scholar
• Ma AT, McAuley S, Pukatzki S, Mekalanos JJ. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 2009; 5(3):234-43; PMID:19286133; https://doi.org/10.1016/j.chom.2009.02.005
   PubMed Web of Science ®Google Scholar
• Dubytska LP, Rogge ML, Thune RL. Identification and characterization of putative translocated effector proteins of the Edwardsiella ictaluri type III secretion system. mSphere 2016; 1(3):e00039-16; PMID:27303737; https://doi.org/10.1128/mSphere.00039-16
   PubMed Web of Science ®Google Scholar
• Wang B, Mo ZL, Xiao P, Li J, Zou YX, Hao B, Li GY. EseD, a putative T3SS translocon component of Edwardsiella tarda, contributes to virulence in fish and is a candidate for vaccine development. Mar Biotechnol 2010; 12(6):678-85; PMID:20072793; https://doi.org/10.1007/s10126-009-9255-5
   PubMed Web of Science ®Google Scholar
• Xiao J, Wang Q, Liu Q, Xu L, Wang X, Wu H, Zhang Y. Characterization of Edwardsiella tarda rpoS: effect on serum resistance, chondroitinase activity, biofilm formation, and autoinducer synthetases expression. Appl Microbiol Biotechnol 2009; 83(1):151-60; PMID:19283379; https://doi.org/10.1007/s00253-009-1924-9
   PubMed Web of Science ®Google Scholar
• Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30(15):2114-20; PMID:24695404; https://doi.org/10.1093/bioinformatics/btu170
   PubMed Web of Science ®Google Scholar
• Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25(14):1754-60; PMID:19451168; https://doi.org/10.1093/bioinformatics/btp324
   PubMed Web of Science ®Google Scholar
• Gu D, Guo M, Yang M, Zhang Y, Zhou X, Wang Q. A sigmaE-mediated temperature gauge controls a switch from LuxR-mediated virulence gene expression to thermal stress adaptation in Vibrio alginolyticus. PLoS Pathog 2016; 12(6):e1005645; PMID:27253371; https://doi.org/10.1371/journal.ppat.1005645
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25(4):402-8; PMID:11846609; https://doi.org/10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Fernandez AI, Perez MJ, Rodriguez LA, Nieto TP. Surface phenotypic characteristics and virulence of Spanish isolates of Aeromonas salmonicida after passage through fish. Appl Environ Microbiol 1995; 61(5):2010-12; PMID:7646039
   PubMed Web of Science ®Google Scholar
• Abel S, Abel ZWP, Chang HH, Davis BM, Lipsitch M, Waldor MK. Sequence tag-based analysis of microbial population dynamics. Nat Methods 2015; 12(3):223-6, 3-226; PMID:25599549; https://doi.org/10.1038/nmeth.3253
   PubMed Web of Science ®Google Scholar
• Xiao J, Chen T, Liu B, Yang W, Wang Q, Qu J, Zhang Y. Edwardsiella tarda mutant disrupted in type III secretion system and chorismic acid synthesis and cured of a plasmid as a live attenuated vaccine in turbot. Fish Shellfish Immunol 2013; 35(3):632-41; PMID:23732848; https://doi.org/10.1016/j.fsi.2013.05.022
   PubMed Web of Science ®Google Scholar
• Xiao J, Wang Q, Liu Q, Wang X, Liu H, Zhang Y. Isolation and identification of fish pathogen Edwardsiella tarda from mariculture in China. Aquac Res 2008; 40(1):13-7; https://doi.org/10.1111/j.1365-2109.2008.02101.x
   Web of Science ®Google Scholar
• Dennis JJ, Zylstra GJ. Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl Environ Microbiol 1998; 64(7):2710-5; PMID:9647854
   PubMed Web of Science ®Google Scholar
• Liang W, Wang S, Yu F, Zhang L, Qi G, Liu Y, Gao S, Kan B. Construction and evaluation of a safe, live, oral Vibrio cholerae vaccine candidate, IEM108. Infect Immun 2003; 71(10):5498-504; PMID:14500467; https://doi.org/10.1128/IAI.71.10.5498-5504.2003
   PubMed Web of Science ®Google Scholar
• Milton DL, Norqvist A, Wolf-Watz H. Cloning of a metalloprotease gene involved in the virulence mechanism of Vibrio anguillarum. J Bacteriol 1992: 174(22):7235-44; PMID:1429449; https://doi.org/10.1128/jb.174.22.7235-7244.1992
   PubMed Web of Science ®Google Scholar
• Wang SY, Lauritz J, Jass J, Milton DL. A ToxR homolog from Vibrio anguillarum serotype O1 regulates its own production, bile resistance, and biofilm formation. J Bacteriol 2002; 184(6):1630-9; PMID:11872714; https://doi.org/10.1128/JB.184.6.1630-1639.2002
   PubMed Web of Science ®Google Scholar