Skip to main content

Advertisement

SpringerLink
Log in

Transcriptome Analysis of Two Strains of Proteus mirabilis with Swarming Migration Deficiency Isolated from Patients with Urinary Tract Infection

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Two rare strains of Proteus mirabilis with swarming migration deficiency were isolated from urine samples of two patients with urinary tract infections and were named as G121 and G137. Migration experiments showed that P. mirabilis HI4320 had typical migration on blood agar, while G121 and G137 had significantly weakened migration ability. Results of adhesion tests showed that the adhesion ability of G121 and G137 to the bladder epithelial cell line 5637 was significantly reduced. High-throughput sequencing and alignment analysis of the transcriptomes of the three P. mirabilis strains were conducted, with P. mirabilis HI4320 as the reference strain. Reverse transcription quantitative PCR (RT-qPCR) was used to verify differentially expressed genes. Results of transcriptome analysis and RT-qPCR showed that, compared to the HI4320 strain, genes related to flagellum and fimbria formation, dicarboxylate transport, and cystathionine and anthranilate metabolism were down-regulated in G121 and G137, while genes related to iron transport, molybdenum metabolism, and metalloprotease were up-regulated, suggesting that these genes may be involved in the migration ability and epithelial cell adhesion ability of P. mirabilis. These results provide important insight to the search for virulence genes and the screening of new antibacterial targets for P. mirabilis.

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
Fig. 4

Similar content being viewed by others

References

  1. Hola V, Peroutkova T, Ruzicka F (2012) Virulence factors in Proteus bacteria from biofilm communities of catheter-associated urinary tract infections. FEMS Immunol Med Microbiol 65(2):343–349

    Article  CAS  Google Scholar 

  2. Mobley HL, Belas R (1995) Swarming and pathogenicity of Proteus mirabilis in the urinary tract. Trends Microbiol 3(7):280–284

    Article  CAS  Google Scholar 

  3. Coker C, Poore CA, Li X et al (2000) Pathogenesis of Proteus mirabilis urinary tract infection. Microbes Infect 2(12):1497–1505

    Article  CAS  Google Scholar 

  4. Sabbuba N, Hughes G, Stickler DJ (2002) The migration of Proteus mirabilis and other urinary tract pathogens over Foley catheters. BJU Int 89(1):55–60

    Article  CAS  Google Scholar 

  5. Wray SK, Hull SI, Cook RG et al (1986) Identification and characterization of a uroepithelial cell adhesin from a uropathogenic isolate of Proteus mirabilis. Infect Immun 54(1):43–49

    Article  CAS  Google Scholar 

  6. Bahrani FK, Massad G, Lockatell CV et al (1994) Construction of an MR/P fimbrial mutant of Proteus mirabilis: role in virulence in a mouse model of ascending urinary tract infection. Infect Immun 62(8):3363–3371

    Article  CAS  Google Scholar 

  7. Alavi M, Belas R (2001) Surface sensing, swarmer cell differentiation, and biofilm development. Methods Enzymol 336:29–40

    Article  CAS  Google Scholar 

  8. Liaw SJ, Lai HC, Ho SW et al (2001) Characterisation of p-nitrophenylglycerol-resistant Proteus mirabilis super-swarming mutants. J Med Microbiol 50(12):1039–1048

    Article  CAS  Google Scholar 

  9. Chi F, Wang Y, Gallaher TK et al (2009) Identification of IbeR as a stationary-phase regulator in meningitic Escherichia coli K1 that carries a loss-of-function mutation in rpoS. J Biomed Biotechnol 2009:520283

    Article  Google Scholar 

  10. Fusco A, Savio V, De Filippis A et al (2018) Induction of different apoptosis pathways by two Proteus mirabilis clinical isolates strains in prostatic epithelial cells. Front Physiol 9:1855

    Article  Google Scholar 

  11. Takizawa T, Matsukawa S, Higuchi Y et al (1993) Induction of programmed cell death (apoptosis) by influenza virus infection in tissue culture cells. J Gen Virol 74(Pt 11):2347–2355

    Article  CAS  Google Scholar 

  12. Williams FD, Schwarzhoff RH (1978) Nature of the swarming phenomenon in Proteus. Annu Rev Microbiol 32:101–122

    Article  CAS  Google Scholar 

  13. Rauprich O, Matsushita M, Weijer CJ et al (1996) Periodic phenomena in Proteus mirabilis swarm colony development. J Bacteriol 178(22):6525–6538

    Article  CAS  Google Scholar 

  14. Pearson MM, Yep A, Smith SN et al (2011) Transcriptome of Proteus mirabilis in the murine urinary tract: virulence and nitrogen assimilation gene expression. Infect Immun 79(7):2619–2631

    Article  CAS  Google Scholar 

  15. Lee YY, Belas R (2015) Loss of FliL alters Proteus mirabilis surface sensing and temperature-dependent swarming. J Bacteriol 197(1):159–173

    Article  Google Scholar 

  16. Lee YY, Patellis J, Belas R (2013) Activity of Proteus mirabilis FliL is viscosity dependent and requires extragenic DNA. J Bacteriol 195(4):823–832

    Article  CAS  Google Scholar 

  17. Belas R, Suvanasuthi R (2005) The ability of Proteus mirabilis to sense surfaces and regulate virulence gene expression involves FliL, a flagellar basal body protein. J Bacteriol 187(19):6789–6803

    Article  CAS  Google Scholar 

  18. Pearson MM, Sebaihia M, Churcher C et al (2008) Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J Bacteriol 190(11):4027–4037

    Article  CAS  Google Scholar 

  19. Glavinas H, Krajcsi P, Cserepes J et al (2004) The role of ABC transporters in drug resistance, metabolism and toxicity. Curr Drug Deliv 1(1):27–42

    Article  CAS  Google Scholar 

  20. Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113

    Article  CAS  Google Scholar 

  21. Shukla S, Wu CP, Ambudkar SV (2008) Development of inhibitors of ATP-binding cassette drug transporters: present status and challenges. Expert Opin Drug Metab Toxicol 4(2):205–223

    Article  CAS  Google Scholar 

  22. Borths EL, Locher KP, Lee AT et al (2002) The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter. Proc Natl Acad Sci USA 99(26):16642–16647

    Article  CAS  Google Scholar 

  23. Kathawala RJ, Gupta P, Ashby CJ et al (2015) The modulation of ABC transporter-mediated multidrug resistance in cancer: a review of the past decade. Drug Resist Updat 18:1–17

    Article  Google Scholar 

  24. Locher KP (2004) Structure and mechanism of ABC transporters. Curr Opin Struct Biol 14(4):426–431

    Article  CAS  Google Scholar 

  25. Rice AJ, Park A, Pinkett HW (2014) Diversity in ABC transporters: type I, II and III importers. Crit Rev Biochem Mol Biol 49(5):426–437

    Article  CAS  Google Scholar 

  26. Leimkuhler S (2017) Shared function and moonlighting proteins in molybdenum cofactor biosynthesis. Biol Chem 398(9):1009–1026

    Article  Google Scholar 

  27. Neumann M, Schulte M, Junemann N et al (2006) Rhodobacter capsulatus XdhC is involved in molybdenum cofactor binding and insertion into xanthine dehydrogenase. J Biol Chem 281(23):15701–15708

    Article  CAS  Google Scholar 

  28. Otrelo-Cardoso AR, Schwuchow V, Rodrigues D et al (2014) Biochemical, stabilization and crystallization studies on a molecular chaperone (PaoD) involved in the maturation of molybdoenzymes. PLoS ONE 9(1):e87295

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Prof. Harry L. T. Mobley (Department of Microbiology and Immunology, University of Michigan Medical School) for providing the Proteus mirabilis strain HI4320.

Funding

This study was funded by the National Natural Science Foundation of China (No. 81670637 for Liang Peng) and General Medical Project of Guangzhou Municipal Health Bureau (No. 20171A011300 for Liang Peng).

Author information

Author notes

  1. Liang Peng, Ding-Qiang Chen, Guan-Ming Jiang, Jing-Yi Ou have contributed equally to this work.

Authors and Affiliations

  1. Department of Clinical Laboratory, The Fifth Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510700, Guangdong, China

    Liang Peng, Li-Ting Zeng, Yi Xiao, Qiong-Yan Jiang &  Ning Sun

  2. Department of Laboratory Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, 510282, Guangdong, China

    Ding-Qiang Chen

  3. Department of Clinical Laboratory, The Fifth Affiliated Hospital of Sun Yat-Sen University, Zhuhai, 519000, Guangdong, China

    Guan-Ming Jiang

  4. Department of Clinical Laboratory, Guangzhou No. 8 People’s Hospital, Guangzhou, 510000, Guangdong, China

    Jing-Yi Ou

  5. Intensive Care Unit, Guangdong 999 Brain Hospital, Guangzhou, 510510, Guangdong, China

    Qiao Jiang

  6. Department of Clinical Laboratory, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510700, Guangdong, China

    Ling Yang

Authors
  1. Liang Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ding-Qiang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guan-Ming Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing-Yi Ou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qiao Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Li-Ting Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yi Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qiong-Yan Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ling Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ning Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived and designed the experiments: LP, DQC, LY, NS. Performed the experiments: LP, DQC, GMJ, JYO. Analyzed the data: LP, LY, NS. Contributed reagents/materials/analysis tools: LTZ, YX, QJ, QYJ. Wrote the paper: LP, DQC, LY, NS.

Corresponding authors

Correspondence to Ling Yang or Ning Sun.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interest.

Ethical Approval

All experiments were approved by the Ethics Committee of the Fifth Affiliated Hospital of Guangzhou Medical University.

Informed Consent

Written informed consent has been acquired from all research participants according to the consent procedures approved by the Ethics Committee of the Fifth Affiliated Hospital of Guangzhou Medical University.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peng, L., Chen, DQ., Jiang, GM. et al. Transcriptome Analysis of Two Strains of Proteus mirabilis with Swarming Migration Deficiency Isolated from Patients with Urinary Tract Infection. Curr Microbiol 77, 1381–1389 (2020). https://doi.org/10.1007/s00284-020-01931-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-01931-6

Keywords

Search

Navigation