Comparative Transcriptomic Analyses of Haemophilus parasuis Reveal Differently Expressed Genes among Strains with Different Virulence Degrees.
Journal
Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448
Informations de publication
Date de publication:
Apr 2021
Apr 2021
Historique:
received:
30
06
2020
accepted:
10
02
2021
pubmed:
7
3
2021
medline:
15
5
2021
entrez:
6
3
2021
Statut:
ppublish
Résumé
Haemophilus parasuis is commonly found in the upper respiratory tract of the pigs. Some isolates of H. parasuis can lead to both pneumonia and Glässer's disease of pigs with severe clinical symptoms. The virulence-associated genes for the various degrees of virulence observed in H. parasuis remains poorly understood. In the present study, we identified the differentially expressed genes between YK1603 (non-virulent strain) and XM1602 (moderately virulent strain) or CY1201 (highly virulent strain) of H. parasuis using Illumina sequencing technique. In comparison to YK1603, a total of 195 genes were significantly changed in CY1201, of which 71 genes were up-regulated and 124 genes were down-regulated, whereas 705 genes were significantly changed in XM1602, of which 415 genes were up-regulated and 290 genes were down-regulated. The enriched analysis of Gene Ontology (GO) terms and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways on the differentially expressed genes showed that both enriched main GO terms and KEGG pathways appear to be different between the two kinds of comparision: CY1201 versus YK1603, and XM1602 versus YK1603. Based on real-time PCR technique, on the whole, it was confirmed that the expression of ten genes: lpxL, tbpB, kdtA, waaQ, oapA, napA, ptsH, mmsA, lpxM, and lpxB were agreement with the findings in Illumina sequencing analysis. These identified genes might participate in the regulation of a wide range of biological process involved in virulence of H. parasuis, such as phosphotransferase system and ABC transporters. Our results from this study provide a new way to gain insight into the virulent mechanisms of H. parasuis.
Identifiants
pubmed: 33674900
doi: 10.1007/s00284-021-02417-9
pii: 10.1007/s00284-021-02417-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1566-1576Subventions
Organisme : Zoonosis Research Engineering Laboratory Project of Liaoning Province
ID : 01072917001
Organisme : Natural Science Foundation of Liaoning Province
ID : 1600759135654
Organisme : the Scientific Research Project of Liaoning Provincial Department of Education
ID : LSNJC201917
Références
Howell KJ, Weinert LA, Peters SE, Wang J, Hernandez-Garcia J, Chaudhuri RR, Luan SL, Angen Ø, Aragon V, Williamson SM, Langford PR, Rycroft AN, Wren BW, Maskell DJ, Tucker AW (2017) “Pathotyping” Multiplex PCR Assay for Haemophilus parasuis: a Tool for Prediction of Virulence. J Clin Microbiol 55(9):2617–2628
doi: 10.1128/JCM.02464-16
Oliveira S, Pijoan C (2004) Haemophilus parasuis: new trends on diagnosis, epidemiology and control. Vet Microbiol 99:1–12
doi: 10.1016/j.vetmic.2003.12.001
Smart NL, Miniats OP, Rosendal S, Friendship RM (1989) Glasser’s disease and prevalence of subclinical infection with Haemophilus parasuis in swine in southern Ontario. Can Vet J 30:339–343
pubmed: 17423292
pmcid: 1681197
Yu J, Wu J, Zhang Y, Du Y, Peng J, Chen L, Sun W, Cong X, Xu S, Shi J, Li J, Huang B, Zhu X, Wang J (2014) Identification of putative virulence-associated genes among Haemophilus parasuis strains and the virulence difference of different serovars. Microb Pathog 77:17–23
doi: 10.1016/j.micpath.2014.10.001
Kielstein P, Rapp-Gabrielson VJ (1992) Designation of 15 serovars of Haemophilus parasuis on the basis of immunodiffusion using heat-stable antigen extracts. J Clin Microbiol 30:862–865
doi: 10.1128/JCM.30.4.862-865.1992
Oliveira S, Blackall PJ, Pijoan C (2003) Characterization of the diversity of Haemophilus parasuis field isolates by use of serotyping and genotyping. Am J Vet Res 64:435–442
doi: 10.2460/ajvr.2003.64.435
Turni C, Blackall PJ (2005) Comparison of the indirect haemagglutination and gel diffusion test for serotyping Haemophilus parasuis. Vet Microbiol 106:145–151
doi: 10.1016/j.vetmic.2004.12.019
Turni C, Singh R, Blackall PJ (2018) Virulence-associated gene profiling, DNA fingerprinting and multilocus sequence typing of Haemophilus parasuis isolates in Australia. Aust Vet J 96(6):196–202
doi: 10.1111/avj.12705
Taylor JE, Swiderska A, Artero JB, Callow P, Kneale G (2012) Structural and functional analysis of the symmetrical type I restriction endonuclease R.EcoR1241NT. PLoS ONE 7:e35263
doi: 10.1371/journal.pone.0035263
Zhou H, Yang B, Xu F, Chen X, Wang J, Blackall PJ, Zhang P, Xia Y, Zhang J, Ma R (2010) Identification of putative virulence-associated genes of Haemophilus parasuis through suppression subtractive hybridization. Vet Microbiol 144:377–383
doi: 10.1016/j.vetmic.2010.01.023
Ruiz A, Oliveira S, Torremorell M, Pijoan C (2001) Outer membrane proteins and DNA profiles in strains of Haemophilus parasuis recovered from systemic and respiratory sites. J Clin Microbiol 39(5):1757–1762
doi: 10.1128/JCM.39.5.1757-1762.2001
Wang X, Xu X, Zhang S, Guo F, Cai X, Chen H (2011) Identification and analysis of potential virulence-associated genes in Haemophilus parasuis based on genomic subtraction. Microb Pathog 51:291–296
doi: 10.1016/j.micpath.2011.06.007
Zhang B, He Y, Xu C, Xu L, Feng S, Liao M, Ren T (2012) Cytolethal distending toxin (CDT) of the Haemophilus parasuis SC096 strain contributes to serum resistance and adherence to and invasion of PK-15 and PUVEC cells. Vet Microbiol. 157:237–242
doi: 10.1016/j.vetmic.2011.12.002
Wang C, Chen F, Hu H, Li W, Wang Y, Chen P, Liu Y, Ku X, He Q, Chen H, Xue F (2014) Gene expression profiling of Cecropin B-resistant Haemophilus parasuis. J Mol Microbiol Biotechnol 24:120–129
doi: 10.1159/000362277
Volokhov DV, Kong H, Herold K, Chizhikov VE, Rasooly A (2011) Oligonucleotide microarrays for identification of microbial pathogens and detection of their virulence-associated or drug-resistance determinants. Methods Mol Biol 671:55–94
doi: 10.1007/978-1-59745-551-0_3
Oliveira S, Galina L, Pijoan C (2001) Development of a PCR test to diagnose Haemophilus parasuis infections. J Vet Diagn Invest 13:495–501
doi: 10.1177/104063870101300607
Howell KJ, Peters SE, Wang J, Hernandez-Garcia J, Weinert LA, Luan SL, Chaudhuri RR, Angen Ø, Aragon V, Williamson SM, Parkhill J, Langford PR, Rycroft AN, Wren BW, Maskell DJ, Tucker AW, BRaDP1T Consortium (2015) Development of a Multiplex PCR Assay for Rapid Molecular Serotyping of Haemophilus parasuis. J Clin Microbiol. 53(12):3812–3821
doi: 10.1128/JCM.01991-15
Jin H, Wan Y, Zhou R, Li L, Luo R, Zhang S, Hu J, Langford PR, Chen H (2008) Identification of gene transcribed by Haemophilus parasuis in necrotic porcine lung through the selective capture of transcribed sequences (SCOTS). Environ Microbiol 10:3326–3336
doi: 10.1111/j.1462-2920.2008.01729.x
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140
doi: 10.1093/bioinformatics/btp616
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods 25(4):402–408
doi: 10.1006/meth.2001.1262
Lei Z, Fu S, Yang B, Liu Q, Ahmed S, Xu L, Xiong J, Cao J, Qiu Y (2017) Comparative transcriptional profiling of tildipirosin-resistant and sensitive Haemophilus parasuis. Sci Rep 7:7517
doi: 10.1038/s41598-017-07972-5
Postma PW, Lengeler JW, Jacobson GR (1993) Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57:543–594
doi: 10.1128/MR.57.3.543-594.1993
Zúñiga M, Comas I, Linaje R, Monedero V, Yebra MJ, Esteban CD, Deutscher J, Pérez-Martínez G, González-Candelas F (2005) Horizontal gene transfer in the molecular evolution of mannose PTS transporters. Mol Biol Evol 22:1673–1685
doi: 10.1093/molbev/msi163
Dennis PP (1976) Effects of chloramphenicol on the transcriptional activities of ribosomal RNA and ribosomal protein genes in Escherichia coli. J Mol Biol 108:535–546
doi: 10.1016/S0022-2836(76)80135-0
Tjalsma H, Bolhuis A, Jongbloed JDH, Bron S, van Dijl JM (2000) Signal peptide-dependent protein transport in Bacillus subtilis:a genome-based survey of the secretome. Microbiol Mol Biol Rev 64(3):515–547
doi: 10.1128/MMBR.64.3.515-547.2000
Mendez C, Salas JA (1998) ABC transporters in antibiotic-producing actinomycetes. FEMS Microbiol Lett 158:1–8
doi: 10.1016/S0378-1097(97)00434-5
Mendez C, Salas JA (2001) The role of ABC transporters in antibiotic-producing organisms: drug secretion and resistance mechanisms. Res Microbiol 152:341–350
doi: 10.1016/S0923-2508(01)01205-0
Calmettes C, Yu RH, Silva LP, Curran D, Schriemer DC, Schryvers AB, Moraes TF (2011) Structural variations within the transferrin binding site on transferrin-binding protein B. TbpB J Biol Chem 286(14):12683–12692
doi: 10.1074/jbc.M110.206102
Kim JS, Kim WS, Choi HH et al (2015) Mycobacterium tuberculosis MmsA, a novel immunostimulatory antigen, induces dendritic cell activation and promotes Th1 cell-type immune responses. Cell Immunol 298(1–2):115–125
doi: 10.1016/j.cellimm.2015.10.005
Mills G, Dumigan A, Kidd T, Hobley L, Bengoechea JA (2017) Identification and Characterization of Two Klebsiella pneumoniae lpxL Lipid A Late Acyltransferases and Their Role in Virulence. Infect Immun. https://doi.org/10.1128/IAI.00068-17
doi: 10.1128/IAI.00068-17
pubmed: 28652313
pmcid: 5563558
Needham BD, Carroll SM, Giles DK, Georgiou G, Whiteley M, Trent MS (2013) Modulating the innate immune response by combinatorial engineering of endotoxin. Proc Natl Acad Sci USA 110:1464–1469
doi: 10.1073/pnas.1218080110
Piya MK, McTernan PG, Kumar S (2013) Adipokine inflammation and insulin resistance: the role of glucose, lipids and endotoxin. J Endocrinol 216(1):T1–T15
doi: 10.1530/JOE-12-0498
Xia D, Samols D (1997) Transgenic mice expressing rabbit C-reactive protein are resistant to endotoxemia. Proc Natl Acad Sci USA 94:2575–2580
doi: 10.1073/pnas.94.6.2575
Chandran SS, Yi J, Draths KM, von Daeniken R, Weber W, Frost JW (2003) Phosphoenolpyruvate availability and the biosynthesis of shikimic acid. Biotechnol Prog 19(3):808–814
doi: 10.1021/bp025769p
Simon J, Sänger M, Schuster SC, Gross R (2003) Electron transport to periplasmic nitrate reductase (NapA) of Wolinella succinogenes is independent of a NapC protein. Mol Microbiol 49(1):69–79
doi: 10.1046/j.1365-2958.2003.03544.x
Xu C, Zhang L, Zhang B, Feng S, Zhou S, Li J, Zou Y, Liao M (2013) Involvement of lipooligosaccharide heptose residues of Haemophilus parasuis SC096 strain in serum resistance, adhesion and invasion. Vet J 195(2):200–204
doi: 10.1016/j.tvjl.2012.06.017
Bohl TE, Shi K, Lee JK, Aihara H (2018) Crystal structure of lipid A disaccharide synthase LpxB from Escherichia coli. Nat Commun 9(1):377
doi: 10.1038/s41467-017-02712-9
Metzger LE, Raetz CR (2009) Purification and characterization of the lipid A disaccharide synthase (LpxB) from Escherichia coli, a peripheral membrane protein. Biochemistry 48:11559–11571
doi: 10.1021/bi901750f
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323
doi: 10.1186/1471-2105-12-323