Skip to main content

Advertisement

SpringerLink
Log in

Regulators of natural competence in Vibrio parahaemolyticus

  • Environmental Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Vibrio parahaemolyticus can degrade insoluble chitin with the help of chitinase enzymes that generate soluble N-acetyl glucosamine oligosaccharides (GlcNAcn) to induce a state of natural competence for the uptake of extracellular DNA. In this study, we had evaluated the role of various regulatory factors such as TfoX, CytR, OpaR, and RpoS during natural transformation of V. parahaemolyticus. The results suggest that TfoX regulates natural competence via CytR in a chitin-dependent manner. CytR controls the release of GlcNAc6 from insoluble chitin and conversion of GlcNAc6 into smaller GlcNAc residues inside the periplasm by modulating the expression of endochitinase and periplasmic chitinases. In addition, CytR was also responsible for GlcNAc6-mediated upregulation of competence-related genes such as pilA, pilB, comEA, and qstR. Next, we found that the quorum sensing regulator OpaR affects the natural transformation through its regulation of extracellular nuclease Dns. The ΔopaR mutant showed increased expression of Dns, which might degrade the eDNA. As a consequence, the transformation efficiency was decreased and eDNA-dependent growth was hugely enhanced. However, when Dns-containing DASW was substituted with fresh DASW, the transformation was detectable in ΔopaR mutant and eDNA-dependent growth was less. These results suggest that the occurrence of natural transformation and eDNA-dependent growth were inversely related to each other. Lastly, the general stress regulator RpoS was required for neither quorum-sensing dependent nor chitin-dependent regulation of natural competence 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

References

  1. Meibom KL, Blokesch M, Dolganov NA, Wu CY, Schoolnik GK (2005) Chitin induces natural competence in Vibrio cholerae. Science 310:1824–1827

    Article  CAS  Google Scholar 

  2. Gulig PA, Tucker MS, Thiaville PC, Joseph JL, Brown RN (2009) USER friendly cloning coupled with chitin-based natural transformation enables rapid mutagenesis of Vibrio vulnificus. Appl Environ Microbiol 75:4936–4949

    Article  CAS  Google Scholar 

  3. Pollack-Berti A, Wollenberg MS, Ruby EG (2010) Natural transformation of Vibrio fischeri requires tfoX and tfoY. Environ Microbiol 12:2302–2311

    PubMed  PubMed Central  Google Scholar 

  4. Chen Y, Dai J, Morris JG Jr, Johnson JA (2010) Genetic analysis of the capsule polysaccharide (K antigen) and exopolysaccharide genes in pandemic Vibrio parahaemolyticus O3:K6. BMC Microbiol 10:274

    Article  Google Scholar 

  5. Vorkapic D, Pressler K, Schild S (2016) Multifaceted roles of extracellular DNA in bacterial physiology. Curr Genet 62(1):71–79

    Article  CAS  Google Scholar 

  6. Sun Y, Bernardy EE, Hammer BK, Miyashiro T (2013) Competence and natural transformation in Vibrios. Mol Microbiol 89(4):583–595

    Article  CAS  Google Scholar 

  7. Yamamoto S, Mitobe J, Ishikawa T, Wai SN, Ohnishi M, Watanabe H, Izumiya H (2014) Regulation of natural competence by the orphan two-component system sensor kinase ChiS involves a non-canonical transmembrane regulator in V. cholerae. Mol Microbiol 91:326–347

    Article  CAS  Google Scholar 

  8. Dalia AB, Lazinski DW, Camilli A (2014) Identification of a membrane-bound transcriptional regulator that links chitin and natural competence in Vibrio cholerae. mBio 5:e01028-13

    Article  Google Scholar 

  9. Dalia AB (2016) RpoS is required for natural transformation of Vibrio cholerae through regulation of chitinases. Environ Microbiol 18(11):3758–3767

    Article  CAS  Google Scholar 

  10. Watve SS, Thomas J, Hammer BK (2015) CytR is a global positive regulator of competence, type VI secretion, and chitinases in Vibrio cholerae. PLoS ONE 10(9):e0138834

    Article  Google Scholar 

  11. Blokesch M, Schoolnik GK (2008) The extracellular nuclease Dns and its role in natural transformation of Vibrio cholerae. J Bacteriol 190(21):7232–7240

    Article  CAS  Google Scholar 

  12. Debnath A, Mizuno T, Miyoshi SI (2020) Regulation of chitin-dependent growth and natural competence in Vibrio parahaemolyticus. Microorganisms 8:E1303

    Article  Google Scholar 

  13. Hirano T, Okubo M, Tsuda H, Yokoyama M, Hakamata W, Nishio T (2019) Chitin heterodisaccharide, released from chitin by chitinase and chitin oligosaccharide deacetylase, enhances the chitin-metabolizing ability of Vibrio parahaemolyticus. J Bacteriol 201:e00270-e319

    Article  CAS  Google Scholar 

  14. Wong HC, Liu SH, Wang TK, Lee CL, Chiou CS, Liu DP, Nishibuchi M, Lee BK (2000) Characteristics of Vibrio parahaemolyticus O3:K6 from Asia. Appl Environ Microbiol 66:3981–3986

    Article  CAS  Google Scholar 

  15. Kuroda T, Mizushima T, Tsuchiya T (2005) Physiological roles of three Na+/H+ antiporters in the halophilic bacterium Vibrio parahaemolyticus. Microbiol Immunol 49:711–719

    Article  CAS  Google Scholar 

  16. Makino K, Oshima K, Kurokawa K, Yokoyama K, Uda T, Tagomori K, Iijima Y, Najima M, Nakano M, Yamashita A, Kubota Y, Kimura S, Yasunaga T, Honda T, Shinagawa H, Hattori M, Iida T (2003) Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361:743–749

    Article  CAS  Google Scholar 

  17. Lin YH, Miyamoto C, Meighen EA (2002) Cloning, sequencing, and functional studies of the rpoS gene from Vibrio harveyi. Biochem Biophys Res Commun 293:456–462

    Article  CAS  Google Scholar 

  18. Yamamoto S, Izumiya H, Mitobe J, Morita M, Arakawa E, Ohnishi M, Watanabe H (2011) Identification of a chitin-induced small RNA that regulates translation of tfoX gene, encoding a positive regulator of natural competence in V. cholerae. J Bacteriol 193:1953–1965

    Article  CAS  Google Scholar 

Download references

Funding

This investigation is supported by the Japan Initiative for Global Research Network on Infectious Diseases (J-GRID; JP20wm0125004) from Ministry of Education, Culture, Sport, Science and Technology in Japan (MEXT) and Japan Agency for Medical Research and Development (AMED). The funders had no role in study design, data collection and analysis, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, 1-1-1, Tsushimanaka, Kita-ku, Okayama, 700-8530, Japan

    Anusuya Debnath & Shin-Ichi Miyoshi

  2. Department of Biotechnology, Brainware University, Kolkata, India

    Anusuya Debnath

Authors
  1. Anusuya Debnath
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shin-Ichi Miyoshi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anusuya Debnath.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

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

Responsible Editor: Cristiano Gallina Moreira

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Debnath, A., Miyoshi, SI. Regulators of natural competence in Vibrio parahaemolyticus. Braz J Microbiol 53, 1491–1499 (2022). https://doi.org/10.1007/s42770-022-00788-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-022-00788-0

Keywords

Search

Navigation