Skip to main content
SpringerLink
Log in

Transcriptional responses of Haemophilus parasuis to iron-restriction stress in vitro

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Haemophilus parasuis is the causative agent of Glässer’s disease, which is responsible for the increasing economic losses in the pig industry worldwide. In this study, selective capture of transcribed sequences approach was used to investigate the transcriptional responses of H. parasuis to iron-restriction stress. Thirty-six genes were identified to be up-regulated under iron-restricted conditions. Knowledge of the genes involved in adaptation to environments encountered during disease will help understand the mechanisms of pathogenesis for this economically significant bacterium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bassler BL (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 2:582–587. doi:10.1016/S1369-5274(99)00025-9

    Article  CAS  PubMed  Google Scholar 

  • Bauer BA, Stevens MK, Hansen EJ (1998) Involvement of the Haemophilus ducreyi gmhA gene product in lipooligosaccharide expression and virulence. Infect Immun 66:4290–4298

    CAS  PubMed  Google Scholar 

  • Bearden SW, Staggs TM, Perry RD (1998) An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J Bacteriol 180(5):1135–1147

    CAS  PubMed  Google Scholar 

  • Braun V (2001) Iron uptake mechanisms and their regulation in pathogenic bacteria. Int J Med Microbiol 291(2):67–79. doi:10.1078/1438-4221-00103

    Article  CAS  PubMed  Google Scholar 

  • Brooke JS, Valvano MA (1996) Biosynthesis of inner core lipopolysaccharide in enteric bacteria: identification and characterization of a conserved phosphoheptose isomerase. J Biol Chem 271:1–7

    Google Scholar 

  • Cai X, Chen H, Blackall PJ, Yin Z, Wang L, Liu Z, Jin M (2005) Serological characterization of Haemophilus parasuis isolates from China. Vet Microbiol 111:231–236

    Article  PubMed  Google Scholar 

  • del Río ML, Gutiérrez-Martín CB, Rodríguez-Barbosa JI, Navas J, Rodrígue z-Ferri EF (2005) Identification and characterization of the TonB region and its role in transferrin-mediated iron acquisition in Haemophilus parasuis. FEMS Immunol Med Microbiol 45(1):75–86. doi:10.1016/j.femsim.2005.02.008

    Article  PubMed  Google Scholar 

  • Deslandes V, Nash JH, Harel J, Coulton JW, Jacques M (2007) Transcriptional profiling of Actinobacillus pleuropneumoniae under iron-restricted conditions. BMC Genomics 8:72. doi:10.1186/1471-2164-8-72

    Article  PubMed  Google Scholar 

  • Fong KP, Gao L, Demuth DR (2003) luxS and arcB control aerobic growth of Actinobacillus actinomycetemcomitans under iron limitation. Infect Immun 71:298–308. doi:10.1128/IAI.71.1.298-308.2003

    Article  CAS  PubMed  Google Scholar 

  • Froussard P (1992) A random-PCR method (rPCR) to construct whole cDNA library from low amounts of RNA. Nucleic Acids Res 20:2900. doi:10.1093/nar/20.11.2900

    Article  CAS  PubMed  Google Scholar 

  • Georgellis D, Kwon O, Lin ECC, Wong SM, Akerley BJ (2001) Redox signal transduction by the ArcB sensor kinase of Haemophilus influenzae lacking the PAS domain. J Bacteriol 183:7206–7212. doi:10.1128/JB.183.24.7206-7212.2001

    Article  CAS  PubMed  Google Scholar 

  • Graham JE, Clark-Curtiss JE (1999) Identification of Mycobacterium tuberculosis RNAs synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proc Natl Acad Sci USA 96:11554–11559. doi:10.1073/pnas.96.20.11554

    Article  CAS  PubMed  Google Scholar 

  • Hoefling DC (1991) Acute myositis associated with Haemophilus parasuis in primary SPF sows. J Vet Diagn Invest 3:354–355

    CAS  PubMed  Google Scholar 

  • Hou JY, Graham JE, Clark-Curtiss JE (2002) Mycobacterium avium genes expressed during growth in human macrophages detected by selective capture of transcribed sequences (SCOTS). Infect Immun 70:3714–3726. doi:10.1128/IAI.70.7.3714-3726.2002

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Wan Y, Zhou R, Luo R, Li L, Zhang S, Hu J, Langford PR, Chen H (2008) Identification of genes transcribed by Haemophilus parasuis in necrotic porcine lung through the Selective Capture of Transcribed Sequences (SCOTS). Environ Microbiol 10(12):3326–3336

    Article  CAS  PubMed  Google Scholar 

  • Jurcisek JA, Bakaletz LO (2007) Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J Bacteriol 189:3868–3875. doi:10.1128/JB.01935-06

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lee S, Sowa ME, Watanabe YH, Sigler PB, Chiu W, Yoshida M, Tsail FTF (2003) The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115(2):229–240. doi:10.1016/S0092-8674(03)00807-9

    Article  CAS  PubMed  Google Scholar 

  • Luke NR, Howlett AJ, Shao J, Campagnari AA (2004) Expression of type IV pili by Moraxella catarrhalis is essential for natural competence and is affected by iron limitation. Infect Immun 72:6262–6270. doi:10.1128/IAI.72.11.6262-6270.2004

    Article  CAS  PubMed  Google Scholar 

  • Melnikow E, Dornan S, Sargent C, Duszenko M, Evans G, Gunkel N, Selzer PM, Ullrich HJ (2005) Microarray analysis of Haemophilus parasuis gene expression under in vitro growth conditions mimicking the in vivo environment. Vet Microbiol 110:255–263. doi:10.1016/j.vetmic.2005.08.007

    Article  CAS  PubMed  Google Scholar 

  • Metcalf DS, MacInnes JI (2007) Differential expression of Haemophilus parasuis genes in response to iron restriction and cerebrospinal fluid. Can J Vet Res 71(3):181–188

    CAS  PubMed  Google Scholar 

  • Mey AR, Wyckoff EE, Kanukurthy V, Fisher CR, Payne SM (2005) Iron and fur regulation in Vibrio cholerae and the role of fur in virulence. Infect Immun 73:8167–8178. doi:10.1128/IAI.73.12.8167-8178.2005

    Article  CAS  PubMed  Google Scholar 

  • Münch R, Hiller K, Grote A, Scheer M, Klein J, Schobert M, Jahn D (2005) Virtual footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Bioinformatics 21:4187–4189. doi:10.1093/bioinformatics/bti635

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Paranjpye RN, Strom MS (2005) A Vibrio vulnificus Type IV pilin contributes to biofilm formation, adherence to epithelial cells and virulence. Infect Immun 73:1411–1422. doi:10.1128/IAI.73.3.1411-1422.2005

    Article  CAS  PubMed  Google Scholar 

  • Paustian ML, May BJ, Kapur V (2001) Pasteurella multocida gene expression in response to iron limitation. Infect Immun 69:4109–4115. doi:10.1128/IAI.69.6.4109-4115.2001

    Article  CAS  PubMed  Google Scholar 

  • Sebastian S, Agarwal S, Murphy JR, Genco CA (2002) The gonococcal fur regulon: identification of additional genes involved in major catabolic, recombination, and secretory pathways. J Bacteriol 184:3965–3974. doi:10.1128/JB.184.14.3965-3974.2002

    Article  CAS  PubMed  Google Scholar 

  • Sritharan M (2006) Iron and bacterial virulence. Int J Med Microbiol 24:163–164

    CAS  Google Scholar 

  • Stohl EA, Seifert HS (2006) Neisseria gonorrhoeae DNA recombination and repair enzymes protect against oxidative damage caused by hydrogen peroxide. J Bacteriol 188:7645–7651. doi:10.1128/JB.00801-06

    Article  CAS  PubMed  Google Scholar 

  • Taha MK, Dupuy B, Saurin W, So M, Marchal C (1991) Control of pilus expression in Neisseria gonorrhoeae as an original system in the family of two-component regulators. Mol Microbiol 5(1):137–148. doi:10.1111/j.1365-2958.1991.tb01834.x

    Article  CAS  PubMed  Google Scholar 

  • Taha MK, Larribe M, Dupuy B, Giorgini D, Marchal C (1992) Role of pilA, an essential regulatory gene of Neisseria gonorrhoeae, in stress response. J Bacteriol 174:5978–5981

    CAS  PubMed  Google Scholar 

  • Turner AK, Lovell MA, Hulme SD, Zhang-Barber L, Barrow PA (1998) Identification of Salmonella typhimurium genes required for colonization of the chicken alimentary tract and for virulence in newly hatched chicks. Infect Immun 66:2099–2106

    CAS  PubMed  Google Scholar 

  • Wandersman C, Stojiljkovic I (2000) Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr Opin Microbiol 3(2):215–220. doi:10.1016/S1369-5274(00)00078-3

    Article  CAS  PubMed  Google Scholar 

  • Xavier Karina B, Bassler BonnieL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6:191–197. doi:10.1016/S1369-5274(03)00028-6

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Basic Research Program of China (973 Program, 2006CB504402), Cultivation Fund of the Key Scientific and Technical Innovation Project from China Ministry of Education (706042), Hi-Tech Research and Development Program of China (863 Program, 2008AA022134), National Scientific and Technical Supporting Program of China (2006BAD06A01), and Hubei Natural Science Foundation (2007ABB015).

Author information

Authors and Affiliations

  1. Division of Animal Infectious Disease, State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, 430070, Wuhan, China

    Qiyun Xie, Hui Jin, Rui Luo, Yun Wan, Jie Chu, Hufeng Zhou, Bi Shi, Huanchun Chen & Rui Zhou

Authors
  1. Qiyun Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hui Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rui Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yun Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jie Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hufeng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bi Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Huanchun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rui Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rui Zhou.

Additional information

Q. Xie and H. Jin contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xie, Q., Jin, H., Luo, R. et al. Transcriptional responses of Haemophilus parasuis to iron-restriction stress in vitro. Biometals 22, 907–916 (2009). https://doi.org/10.1007/s10534-009-9243-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-009-9243-2

Keywords

Search

Navigation