Skip to main content
SpringerLink
Log in

The first report on Listeria monocytogenes producing siderophores and responds positively to N-acyl homoserine lactone (AHL) molecules by enhanced biofilm formation

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Listeria monocytogenes are Gram-positive well-known emerging food-borne pathogens causing listeriosis in humans. In the present study, we have isolated biofilm-forming Listeria sp. from utensils used by a local milk collection dairy society at Usgao Goa, which collects milk for Goa dairy. Through biochemical tests and 16S rRNA sequence analysis, the bacterium was confirmed to be L. monocytogenes and designated as strain BN3, having GenBank accession number MF095110. We report for the first time Gram-positive L. monocytogenes strain BN3 producing iron-chelating siderophores by chrome azurol S (CAS) agar test. Also, this is a first report which reveals that L. monocytogenes strain BN3 responds to N-hexanoyl-homoserine lactone molecule (C6-HSL) by gradual increase in their biofilm-forming potential with a gradual increase in AHL (C6-HSL) concentration (250, 500 nM–1 μM) as compared to control revealed by crystal violet assay (CV) in microtiter plate. These results were further confirmed by scanning electron microscopy (SEM). A significant decrease in biofilm formation was observed when L. monocytogenes strain BN3 was treated with 10 µg/ml (R)-2-(2-hydroxynaphthalen-1-yl)thiazolidine-4-carboxylic acid, but when 250 and 500 nM AHL molecules were added, biofilm formation in strain BN3 was found to be enhanced as compared to control even in the presence of antibacterial compound, (R)-2-(2-hydroxynaphthalen-1-yl)thiazolidine-4-carboxylic acid. These results revealed that AHL molecules nullify the effect of antimicrobial compound and promote biofilm formation in L. monocytogenes strain BN3.

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

  • Barchini E, Cowart RE (1996) Extracellular iron reductase activity produced by Listeria monocytogenes. Archiv Microbiol 166:51–57

    Article  CAS  Google Scholar 

  • Bauer AW, Kirby WMM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol 45:493–496

    CAS  PubMed  Google Scholar 

  • Biswa P, Doble M (2013) Production of acylated homoserine lactone by Gram-positive bacteria isolated from marine water. FEMS Microbiol Lett 343:34–41

    Article  CAS  PubMed  Google Scholar 

  • Camejo A, Carvalho F, Reis O, Leitao E, Sousa S, Cabanes D (2011) The arsenal of virulence factors deployed by Listeria monocytogenes to promote its cell infection cycle. Virulence 2:379–394

    Article  PubMed  Google Scholar 

  • Cherifi T, Jacques M, Quessy S, Fravalo P (2017) Impact of nutrient restriction on the structure of Listeria monocytogenes biofilm grown in a microfluidic system. Front Microbiol 8:864. doi:10.3389/fmicb.2017.00864

    Article  PubMed  PubMed Central  Google Scholar 

  • Doijad SP (2014) Biofilm forming ability and disinfectant resistance of Listeria species from food and food processing units. Shodhganga: a reservoir of Indian thesis, 1–221

  • Doijad SP, Vaidya V, Garg S, Kalekar S, Rodrigues J, D’Costa D, Bhosle SN, Barbuddhe SB (2010) Isolation and characterization of Listeria species from raw and processed meats. J Veter Pub Health 8:83–88

    Google Scholar 

  • Doijad S, Barbuddhe SB, Garg S, Kalekar S, Rodrigues J, D’Costa D, Bhosle S, Chakraborty T (2011) Incidence and genetic variability of Listeria species from three milk processing plants. Food Control 22:1900–1904

    Article  Google Scholar 

  • Doijad SP, Barbuddhe SB, Garg S, Poharkar KV, Kalorey DR, Kurkure NV, Rawool DB, Chakraborthy T (2015) Biofilm-forming abilities of Listeria monocytogenes serotypes isolated from different sources. PLoS One 10(9):e0137046. doi:10.1371/journal.pone.0137046

    Article  PubMed  PubMed Central  Google Scholar 

  • Dudhe NC, Chaudhary SP, Pantawane PB, Hirde VN, Ramees TP, Zade NN (2014) In-vitro characterization of Listeria monocytogenes isolates by haemolysis, CAMP, PIPLC assay with protein profiling and antibiotic resistance recovered from Nagpur region. Adv Anim Veter Sci 2:321–328

    Article  Google Scholar 

  • Eide MH, Homleid JP, Mattsson B (2003) Life cycle assessment (LCA) of cleaning-in-place processes in dairies. LWT Food Sci Technol 36:303–314

    Article  CAS  Google Scholar 

  • Farber JM, Peterkin PI (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 55:476–511

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garmyn D, Gal L, Lemaitre J-P, Hartmann A, Piveteau P (2009) Communication and autoinduction in the species Listeria monocytogenes. Commun Integrat Biol 2:371–374

    Article  Google Scholar 

  • Gray B, Hall P, Gresham H (2013) Targeting agr- and agr-like quorum sensing systems for development of common therapeutics to treat multiple Gram-positive bacterial infections. Sensors 13:5130–5166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irie Y, Parsek MR (2008) Quorum sensing and microbial biofilms. In: Romeo T. (ed) Bacterial biofilms. Curr Topics Microbiol Immunol 322: 67–84

  • Jain AB, Vaidya A, Ravichandran V, Kashaw SK, Agrawal RK (2012) Recent developments and biological activities of thiazolidinone derivatives: a review. Bioorg Med Chem 20:3378–3395

    Article  CAS  PubMed  Google Scholar 

  • Lim Y, Ee R, Yin WF, Chan KG (2014) Quorum sensing activity of Aeromonas caviae strain YL12, a bacterium isolated from compost. Sensors 14:7026–7040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Low JC, Donachie W (1997) A review of Listeria monocytogenes and listeriosis. Veter J 153:9–29

    Article  CAS  Google Scholar 

  • Malik SVS, Barbuddhe SB, Chaudhari SP (2002) Listeric infections in humans and animals in Indian subcontinent: a review. Trop Anim Health Prod 34:359–381

    Article  CAS  PubMed  Google Scholar 

  • Naik MM, Dubey SK (2011) Lead-enhanced siderophore production and alteration in cell morphology in a Pb-resistant Pseudomonas aeruginosa strain 4EA. Curr Microbiol 62:409–414

    Article  CAS  PubMed  Google Scholar 

  • Novick RP, Muir TW (1999) Virulence gene regulation by peptides in staphylococci and other Gram positive bacteria. Curr Opin Microbiol 2:40–45

    Article  CAS  PubMed  Google Scholar 

  • Oliveira MMM, Brugnera DF, Alves E, Piccoli RH (2010) Biofilm formation by Listeria monocytogenes on stainless steel surface and biotransfer potential. Braz J Microbiol 41:97–106

    Article  PubMed  PubMed Central  Google Scholar 

  • Qazi S, Middlenton B, Muharram SH, Cockayne A, Hill P, O’Shea P, Chhabra SR, Camera M, Williams P (2006) N-Acylhomoserine lactones antagonise virulence gene expression and quorum sensing in Staphylococcus aureus. Infect Immun 2006:910–919

    Article  Google Scholar 

  • Raorane AV, Doijad SP, Poharkar KV, Pathak A, Bhosle S, Barbuddhe SB (2015) Isolation and genotypic characterization of Listeria monocytogenes from pork and pork products. Internet J Curr Microbiol Appl Sci 4:788–798

    Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  • Simon N, Coulanges V, Andre P, Vidom DJM (1995) Utilization of exogenous siderophores and natural catechols by Listeria monocytogenes. Appl Environ Microbiol 61:1643–1645

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sneath PHA, Mair NS, Sharpe ME, Holt JG (1986) Bergey’s manual of systematic bacteriology, vol 2. Williams and Wilkins, Baltimore

    Google Scholar 

  • Soyano A, Gomez M (1999) Role of iron in immunity and its relation with infections. Arch Latinoam Nutr 49:40S–46S

    CAS  PubMed  Google Scholar 

  • Swaminathan B, Gerner-Smidt P (2007) The epidemiology of human listeriosis. Microbes Infect 9:1236–1243

    Article  PubMed  Google Scholar 

  • Vázquez-Boland JA, Kuhn M, Berche P, Chakraborthy T, Domínguez-Bernal G, Goebel W, González-Zorn B, Wehland J, Kreft J (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584–640

    Article  PubMed  PubMed Central  Google Scholar 

  • Zetzmann M, Sanchez-Kopper A, Waidmann MS, Blombach B, Riedel CU (2016) Identification of agr peptide of Listeria monocytogenes. Front Microbiol 7:989. doi:10.3389/fmicb.2016.00989

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Dr. Milind Mohan Naik thanks the Science and Engineering Research Board (SERB), Department of Science and Technology, Government of India, for financial support by the Young Scientist Project (File Number: YSS/2014/000258). We are thankful to Prof. S. K. Dubey, Department of Microbiology, Goa University, Dr. S. B. Barbuddhe, Principal Scientist, ICAR-National Institute of Biotic Stress Management, Baroda, Raipur, Chhattisgarh, India, and Mr. Satyajeet Kale, Ph.D. student, Department of Microbiology, Goa University, Goa. We are also thankful to Ms. Shivangi P Naik, M.Sc. Microbiology, Goa University, dissertation student, for her help during this research work and Dr. Shyamalina Haldar, postdoctoral fellow, Department of Microbiology, Goa University.

Author information

Authors and Affiliations

  1. Department of Microbiology, Goa University, Goa, India

    Milind Mohan Naik & Purva Bhangui

  2. Department of Chemistry, Goa University, Goa, India

    Chinmay Bhat

Authors
  1. Milind Mohan Naik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Purva Bhangui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chinmay Bhat
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Milind Mohan Naik.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Erko Stackebrandt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 3087 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Naik, M.M., Bhangui, P. & Bhat, C. The first report on Listeria monocytogenes producing siderophores and responds positively to N-acyl homoserine lactone (AHL) molecules by enhanced biofilm formation. Arch Microbiol 199, 1409–1415 (2017). https://doi.org/10.1007/s00203-017-1416-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-017-1416-8

Keywords

Search

Navigation