Skip to main content
Log in

Identification of Quorum Quenching N-Acyl Homoserine Lactonases from Priestia aryabhattai J1D and Bacillus cereus G Isolated from the Rhizosphere

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Several pathogenic bacteria communicate using N-acyl homoserine lactone (AHL) as a quorum sensing (QS) molecule. The process of interfering with the QS system is known as quorum quenching (QQ), it is an effective tool to control QS-dependent virulence in pathogens. In the present study, rhizosphere bacterial isolates were screened for their ability to produce AHL lactonase enzyme as QQ molecules, which hydrolyses AHL signalling molecules and consequently blocks the QS system. Potent N-hexanoyl-l-homoserine lactone (C6HSL) hydrolytic QQ activity was detected in rhizosphere isolates namely Bacillus cereus G and Priestia aryabhattai J1D. The cell-free supernatant of the bacterial isolates indicated a reduction in biofilm formation in the human pathogens Vibrio cholerae, Pseudomonas aeruginosa, and Staphylococcus aureus without inhibiting cells, signifying their biocontrol property. Furthermore, liquid chromatography high resolution mass spectrometry analysis confirmed C6HSL hydrolytic activity by AHL lactonase produced by these rhizosphere isolates. Also, the aiiA homologous gene from the bacterial isolates showed similarity with the aiiA lactonase gene from Bacillus species, which was further confirmed by homology modelling. In silico structure analysis by comparing with the structure of Bacillus revealed the similarity in the active site, indicating the same degradation pattern. Based on available reported data, the present study indicates the first report of the presence of the aiiA lactonase gene in P. aryabhattai.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The datasets generated during and/or analysed during the current study are available from the corresponding author upon reasonable request.

Code Availability

Not applicable.

References

  1. Raafat MM, Ali Tammam M, Ali AE (2019) Quorum quenching activity of Bacillus cereus isolate 30b confers antipathogenic effects in Pseudomonas aeruginosa. Infect Drug Resist 12:1583–1596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Shastry RP, Dolan SK, Abdelhamid Y, Vittal RR, Welch M (2018) Purification and characterisation of a quorum quenching AHL-lactonase from the endophytic bacterium Enterobacter sp. CS66. FEMS Microbiol Lett 365(9):fny054

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31(2):224–245

    Article  CAS  PubMed  Google Scholar 

  4. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21(1):319–346

    Article  CAS  PubMed  Google Scholar 

  5. Diggle SP, Griffin AS, Campbell GS, West SA (2007) Cooperation and conflict in quorum-sensing bacterial populations. Nature 450(7168):411–414

    Article  CAS  PubMed  Google Scholar 

  6. Li X, Jin J, Zhang X et al (2021) Quantifying the optimal strategy of population control of quorum sensing network in Escherichia coli. NPJ Syst Biol Appl 7:35. https://doi.org/10.1038/s41540-021-00196-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Koo H, Allan RN, Howlin RP, Stoodley P, Hall Stoodley L (2017) Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol 15(12):740–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Rasmussen TB, Givskov M (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296(2–3):149–161

    Article  CAS  PubMed  Google Scholar 

  9. Huma N, Shankar P, Kushwah J et al (2011) Diversity and polymorphism in AHL lactonase gene (aiiA) of Bacillus. J Microbiol Biotechnol 21(10):1001–1011

    Article  CAS  PubMed  Google Scholar 

  10. Lin YH, Xu JL, Hu J, Wang LH, Ong SL, Leadbetter JR, Zhang LH (2003) Acyl homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol 47(3):849–860

    Article  PubMed  Google Scholar 

  11. Park SY, Kang HO, Jang HS, Lee JK, Koo BT, Yum DY (2005) Identification of extracellular N-acyl homoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl Environ Microbiol 71(5):2632–2641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Chan KG, Wong CS, Yin WF, Sam CK, Koh CL (2010) Rapid degradation of N-3-oxo-acyl homoserine lactones by a Bacillus cereus isolate from Malaysian rainforest soil. Antonie Van Leeuwenhoek 98(3):299–305

    Article  CAS  PubMed  Google Scholar 

  13. Dong YH, Wang LH, Zhang LH (2007) Quorum-quenching microbial infections: mechanisms and implications. Philos Trans R Soc B Biol Sci 362(1483):1201–1211

    Article  CAS  Google Scholar 

  14. Augustine N, Kumar P, Thomas S (2010) Inhibition of Vibrio cholerae biofilm by AiiA enzyme produced from Bacillus spp. Arch Microbiol 192(12):1019–1022

    Article  CAS  PubMed  Google Scholar 

  15. Bassetti M, Vena A, Croxatto A, Righi E, Guery B (2018) How to manage Pseudomonas aeruginosa infections. Drugs Context 7:212527. https://doi.org/10.7573/dic.212527

    Article  PubMed  PubMed Central  Google Scholar 

  16. Vinoj G, Pati R, Sonawane A, Vaseeharan B (2015) In Vitro cytotoxic effects of gold nanoparticles coated with functional acyl homoserine lactone lactonase protein from Bacillus licheniformis and their antibiofilm activity against Proteus Species. Antimicrob Agents Chemother 59(2):763–771

    Article  PubMed  PubMed Central  Google Scholar 

  17. Luo J, Dong B, Wang K et al (2017) Baicalin inhibits biofilm formation, attenuates the quorum sensing-controlled virulence and enhances Pseudomonas aeruginosa clearance in a mouse peritoneal implant infection model. PLoS ONE 12(4):e0176883. https://doi.org/10.1371/journal.pone.0176883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mani A, Hameed SS, Ramalingam S, Narayanan M (2012) Assessment of quorum quenching activity of Bacillus species against Pseudomonas aeruginosa MTCC 2297. Glob J Pharmacol 8:118–125

    Google Scholar 

  19. Watve S, Barrasso K, Jung SA et al (2020) Parallel quorum-sensing system in Vibrio cholerae prevents signal interference inside the host. PLoS Pathog 16(2):e1008313. https://doi.org/10.1371/journal.ppat.1008313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Alinejad F, Shahryari F, Eini O, Sarafraz Niko F, Shekari A, Setareh M (2020) Screening of quorum-quenching bacteria associated with rhizosphere as biocontrol agents of Pectobacterium carotovorum subsp. Carotovorum. Arch Phytopathol Plant Prot 53(11–12):509–523

    Article  CAS  Google Scholar 

  21. Rajesh PS, Rai VR (2014) Molecular identification of aiiA homologous gene from endophytic Enterobacter species and in silico analysis of putative tertiary structure of AHL-lactonase. Biochem Biophys Res Commun 443(1):290–295

    Article  CAS  PubMed  Google Scholar 

  22. McLean RJC, Pierson LS, Fuqua C (2004) A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 58(3):351–360

    Article  CAS  PubMed  Google Scholar 

  23. Kothari V, Sharma S, Padia D (2017) Recent research advances on Chromobacterium violaceum. Asian Pac J Trop Med 10(8):744–752

    Article  PubMed  Google Scholar 

  24. Ranjani S, Hemalatha S (2022) Triphala decorated multipotent green nanoparticles and its applications. Mater Lett 308:131184. https://doi.org/10.1016/j.matlet.2021.131184

    Article  CAS  Google Scholar 

  25. Rehman ZU, Leiknes T (2018) Quorum quenching bacteria isolated from red sea sediments reduce biofilm formation by Pseudomonas aeruginosa. Front Microbiol 9:1354. https://doi.org/10.3389/fmicb.2018.01354

    Article  PubMed  PubMed Central  Google Scholar 

  26. Rajesh PS, Ravishankar RV (2014) Quorum quenching activity in cell-free lysate of endophytic bacteria isolated from Pterocarpus santalinus Linn. and its effect on quorum sensing regulated biofilm in Pseudomonas aeruginosa PAO1. Microbiol Res 169(7–8):561–569

    Article  CAS  PubMed  Google Scholar 

  27. Vallet I, Diggle SP, Stacey RE et al (2004) Biofilm formation in Pseudomonas aeruginosa: Fimbrial cup gene clusters are controlled by the transcriptional regulator MvaT. J Bacteriol 186(9):2880–2890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Coffey BM, Anderson GG (2014) Biofilm formation in the 96-well microtiter plate Methods. Mol Biol Clifton NJ 1149:631–641

    Google Scholar 

  29. Lázaro-Silva D, De Mattos J, Castro H, Alves G, Amorim L (2015) The use of DNA extraction for molecular biology and biotechnology training: a practical and alternative approach. Creat Educ 6:762–772

    Article  Google Scholar 

  30. Park JM, Shin JH, Lee DW et al (2010) Identification of the lactic acid bacteria in Kimchi according to initial and over-ripened fermentation using PCR and 16S rRNA gene sequence analysis. Food Sci Biotechnol 19(2):541–546

    Article  CAS  Google Scholar 

  31. Eswar N, Webb B, Marti Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A (2007) Comparative protein structure modeling using MODELLER. Curr Protoc Protein Sci. https://doi.org/10.1002/0471140864.ps0209s50

    Article  PubMed  Google Scholar 

  32. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) “PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291

    Article  CAS  Google Scholar 

  33. Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35:W407–W410

    Article  PubMed  PubMed Central  Google Scholar 

  34. Gupta RS, Patel S, Saini N, Chen S (2020) Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species. Int J Syst Evol Microbiol 70(11):5753–5798

    Article  CAS  PubMed  Google Scholar 

  35. Liu D, Lepore BW, Petsko GA et al (2005) Three-dimensional structure of the quorum-quenching N-acyl homoserine lactone hydrolase from Bacillus thuringiensis. Proc Natl Acad Sci USA 102(33):11882–11887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acyl homoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci 97(7):3526–3531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH (2001) Quenching quorum-sensing dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411(6839):813–817

    Article  CAS  PubMed  Google Scholar 

  38. Rosier A, Beauregard PB, Bais HP (2020) Quorum quenching activity of the PGPR Bacillus subtilis UD1022 alters nodulation efficiency of Sinorhizobium meliloti on Medicago truncatula. Front Microbiol 11:596299. https://doi.org/10.3389/fmicb.2020.596299

    Article  PubMed  Google Scholar 

  39. Chankhamhaengdecha S, Hongvijit S, Srichaisupakit A, Charnchai P, Panbangred W (2013) Endophytic actinomycetes: a novel source of potential acyl homoserine lactone degrading enzymes. BioMed Res Int 2013:782847. https://doi.org/10.1155/2013/782847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Vinoj G, Vaseeharan B, Thomas S, Spiers AJ, Shanthi S (2014) Quorum quenching activity of the AHL lactonase from Bacillus licheniformis DAHB1 inhibits Vibrio biofilm formation in vitro and reduces shrimp intestinal colonisation and mortality. Mar Biotechnol 16(6):707–715

    Article  CAS  Google Scholar 

  41. Hentzer M, Givskov M (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112(9):1300–1307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Saurav K, Bar-Shalom R, Haber M et al (2016) In search of alternative antibiotic drugs: quorum quenching activity in sponges and their bacterial isolates. Front Microbiol 7:416. https://doi.org/10.3389/fmicb.2016.00416

    Article  PubMed  PubMed Central  Google Scholar 

  43. Vesuna AP, Nerurkar AS (2020) Bio control impact of AHL degrading actinobacteria on quorum sensing regulated virulence of phytopathogen Pectobacterium carotovorum subsp. carotovorum BR1. Plant Soil 453(1):371–388

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful to the Management of Maharashtra Education Society, The Principal of MES Abasaheb Garware College, Pune and The Head of the department of Microbiology, Abasaheb Garware College, Pune for providing facilities and infrastructure for this research work.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or non-profit sectors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Niranjan Prakashrao Patil.

Ethics declarations

Conflict of interest

The authors do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted.

Ethical Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1365 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shevate, S.N., Shinde, S.S., Bankar, A.V. et al. Identification of Quorum Quenching N-Acyl Homoserine Lactonases from Priestia aryabhattai J1D and Bacillus cereus G Isolated from the Rhizosphere. Curr Microbiol 80, 86 (2023). https://doi.org/10.1007/s00284-023-03186-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03186-3

Navigation