Skip to main content
SpringerLink
Log in

The Effect of Salinity on Biofilm Formation and c-di-GMP Production in Vibrio parahaemolyticus

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Vibrio parahaemolyticus is a moderately halophilic, salt-requiring organism that exhibits optimal growth at approximately 3% salt. Thus, salinity stress is one of the most important stimuli during its lifecycle. The bacterium possesses a strong ability to form biofilms on surfaces, which are thought to be involved in protecting it from adverse environmental conditions. In the present study, salinity-dependent biofilm formation by V. parahaemolyticus was investigated by combining crystal violet staining, colony morphology, intracellular c-di-GMP quantification and quantitative PCR. The results showed that biofilm formation by V. parahaemolyticus was significantly enhanced in low salinity growth conditions and was affected by incubation time. In addition, low salinity reduced intracellular c-di-GMP degradation in V. parahaemolyticus. Transcription of genes encoding ScrABC and ScrG proteins, which are involved in intracellular c-di-GMP metabolism, was inhibited by low salinity growth conditions. Thus, reduced intracellular c-di-GMP degradation in V. parahaemolyticus in low salinity growth conditions may be mediated by repression of scrG and scrABC transcription. Taken together, these results demonstrated for the first time that salinity regulates biofilm formation and c-di-GMP production in V. parahaemolyticus.

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

Data Availability

All data generated or analyzed during this study are included in the manuscript. Further inquiries may be directed to the corresponding authors.

References

  1. Raszl SM, Froelich BA, Vieira CR, Blackwood AD, Noble RT (2016) Vibrio parahaemolyticus and Vibrio vulnificus in South America: water, seafood and human infections. J Appl Microbiol 121(5):1201–1222

    Article  CAS  Google Scholar 

  2. Osei-Adjei G, Huang X, Zhang Y (2018) The extracellular proteases produced by Vibrio parahaemolyticus. World J Microbiol Biotechnol 34(5):68

    Article  Google Scholar 

  3. Whitaker WB, Parent MA, Naughton LM, Richards GP, Blumerman SL, Boyd EF (2010) Modulation of responses of Vibrio parahaemolyticus O3:K6 to pH and temperature stresses by growth at different salt concentrations. Appl Environ Microbiol 76(14):4720–4729

    Article  CAS  Google Scholar 

  4. Yildiz FH, Visick KL (2009) Vibrio biofilms: so much the same yet so different. Trends Microbiol 17(3):109–118

    Article  CAS  Google Scholar 

  5. Ashrafudoulla M, Mizan MFR, Park SH, Ha SD (2021) Current and future perspectives for controlling Vibrio biofilms in the seafood industry: a comprehensive review. Crit Rev Food Sci Nutr 61(11):1827–1851

    Article  CAS  Google Scholar 

  6. Dong X, Zhang Y, Yang R, Xie C, Zhou D (2014) Effect of salinity and temperature on motility of Vibrio parahaemolyticus [in Chinese]. Military Medical Sciences 12:962–964

    Google Scholar 

  7. Enos-Berlage JL, Guvener ZT, Keenan CE, McCarter LL (2005) Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol Microbiol 55(4):1160–1182

    Article  CAS  Google Scholar 

  8. Kim YK, McCarter LL (2007) ScrG, a GGDEF-EAL protein, participates in regulating swarming and sticking in Vibrio parahaemolyticus. J Bacteriol 189(11):4094–4107

    Article  CAS  Google Scholar 

  9. Ferreira RB, Antunes LC, Greenberg EP, McCarter LL (2008) Vibrio parahaemolyticus ScrC modulates cyclic dimeric GMP regulation of gene expression relevant to growth on surfaces. J Bacteriol 190(3):851–860

    Article  CAS  Google Scholar 

  10. Zhang Y, Qiu Y, Gao H, Sun J, Li X, Zhang M, Xue X, Yang W, Ni B, Hu L et al (2021) OpaR controls the metabolism of c-di-GMP in Vibrio parahaemolyticus. 12(1319)

  11. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, Iijima Y, Najima M, Nakano M, Yamashita A et al (2003) Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae. Lancet 361(9359):743–749

    Article  CAS  Google Scholar 

  12. Fang N, Gao H, Wang L, Qu S, Zhang YQ, Yang RF, Zhou DS (2013) Optimized methods for biofilm analysis in Yersinia pestis. Biomed Environ Sci 26(5):408–411

    PubMed  Google Scholar 

  13. Gao H, Ma L, Qin Q, Qiu Y, Zhang J, Li J, Lou J, Diao B, Zhao H, Shi Q et al (2020) Fur represses Vibrio cholerae biofilm formation via direct regulation of vieSAB, cdgD, vpsU, and vpsA-K transcription. Front Microbiol 11:587159

    Article  Google Scholar 

  14. Gao H, Zhang Y, Yang L, Liu X, Guo Z, Tan Y, Han Y, Huang X, Zhou D, Yang R (2011) Regulatory effects of cAMP receptor protein (CRP) on porin genes and its own gene in Yersinia pestis. BMC Microbiol 11:40

    Article  CAS  Google Scholar 

  15. Jenal U, Reinders A, Lori C (2017) Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol 15(5):271–284

    Article  CAS  Google Scholar 

  16. Yang L, Zhan L, Han H, Gao H, Guo Z, Qin C, Yang R, Liu X, Zhou D (2010) The low-salt stimulon in Vibrio parahaemolyticus. Int J Food Microbiol 137(1):49–54

    Article  CAS  Google Scholar 

  17. Kalburge SS, Whitaker WB, Boyd EF (2014) High-salt preadaptation of Vibrio parahaemolyticus enhances survival in response to lethal environmental stresses. J Food Prot 77(2):246–253

    Article  CAS  Google Scholar 

  18. Wong HC, Peng PY, Han JM, Chang CY, Lan SL (1998) Effect of mild acid treatment on the survival, enteropathogenicity, and protein production in Vibrio parahaemolyticus. Infect Immun 66(7):3066–3071

    Article  CAS  Google Scholar 

  19. Karlsen C, Paulsen SM, Tunsjo HS, Krinner S, Sorum H, Haugen P, Willassen NP (2008) Motility and flagellin gene expression in the fish pathogen Vibrio salmonicida: effects of salinity and temperature. Microb Pathog 45(4):258–264

    Article  CAS  Google Scholar 

  20. Larsen MH, Blackburn N, Larsen JL, Olsen JE (2004) Influences of temperature, salinity and starvation on the motility and chemotactic response of Vibrio anguillarum. Microbiology 150(Pt 5):1283–1290

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript

Funding

This study was supported by grants from the National Natural Science Foundation of China (Grant No. 82072239) and the Fundamental Research Funds for the Central Universities (JUSRP121061).

Author information

Author notes

  1. Xue Li and Junfang Sun have contributed equally to this work.

Authors and Affiliations

  1. Department of Clinical Laboratory, Nantong Third Hospital Affiliated to Nantong University, Nantong, 212006, Jiangsu, China

    Xue Li, Junfang Sun, Qimin Wu, Renfei Lu & Yiquan Zhang

  2. School of Medicine, Jiangsu University, Zhenjiang, 212013, Jiangsu, China

    Miaomiao Zhang, Xingfan Xue & Yiquan Zhang

  3. State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, 100071, China

    Wenhui Yang, Zhe Yin & Dongsheng Zhou

Authors
  1. Xue Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junfang Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miaomiao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xingfan Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qimin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wenhui Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhe Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dongsheng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Renfei Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yiquan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YZ, DZ and RL designed, organized and supervised the experiments, interpreted the results and edited the manuscript. XL, JF, MZ, XX and QW performed the laboratory experiments. XL drafted the manuscript.

Corresponding authors

Correspondence to Renfei Lu or Yiquan Zhang.

Ethics declarations

Conflict of interest

The authors declare that there are no conflict of interest regarding the publication of this article.

Ethical Approval

Not applicable.

Code Availability (Software Application or Custom Code)

Not applicable.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, X., Sun, J., Zhang, M. et al. The Effect of Salinity on Biofilm Formation and c-di-GMP Production in Vibrio parahaemolyticus. Curr Microbiol 79, 25 (2022). https://doi.org/10.1007/s00284-021-02723-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-021-02723-2

Search

Navigation