Journal of Consumer Protection and Food Safety

, Volume 13, Issue 3, pp 289–298 | Cite as

Catabolic activity and biofilm formation of foodborne Listeria monocytogenes strains

  • Nowshin Shyara Sharar
  • Lay Ching Chai
  • Kwai Lin Thong
Research article


Listeria monocytogenes is a major foodborne pathogen causing increased morbidity worldwide. It forms resistant biofilm structures in food processing facilities after sanitization, consequently creating a public health concern. Many studies on the metabolism and transmission of L. monocytogenes has provided insights into its intracellular infection process, however there is limited understanding on the substrate utilization of the bacteria. Therefore, the main objective of this study was to investigate the carbon and nitrogen substrate catabolism and the biofilm forming potential of 3 Malaysian L. monocytogenes strains (LM41, LM92 and LM115) previously isolated from ready-to-eat foods. Biolog Phenotype Microarray (PM) system was used to study the catabolic activity of the foodborne strains in 190 carbon and 380 nitrogen sources. PM analysis showed that the carbon and nitrogen catabolic activity of L. monocytogenes strains were considerably limited and these strains utilised Tween 40 and Tween 80, which are commonly used for the sanitation in food and meat processing industries. Furthermore, all 3 strains showed strong biofilm forming potential in nutrient-rich and nutrient-limited media, irrespective of the serogroups. The data generated could be utilised to develop alternative measure to inhibit biofilm formation in L. monocytogenes in the food processing environment.


Biofilm Foodborne pathogen Listeria monocytogenes Phenotype microarray Ready-to-eat food 



We thank University of Malaya for the financial support and research facilities. This study was supported by the High Impact Research Grant UM.C/625/1/HIR/MOE/CHAN/01/02 from University of Malaya. The funders had no role in project design, data collection and analysis, decision to publish or preparation of the manuscript. This work was performed at the Laboratory of Biomedical Science and Molecular Microbiology, Institute of Graduate Studies, University of Malaya.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

3_2018_1169_MOESM1_ESM.pdf (408 kb)
Supplementary material 1 (PDF 408 kb)
3_2018_1169_MOESM2_ESM.pdf (96 kb)
Supplementary material 2 (PDF 95 kb)


  1. Alonso AN, Perry KJ, Regeimbal JM et al (2014) Identification of Listeria monocytogenes determinants required for biofilm formation. PLoS ONE 9(12):1–16. CrossRefGoogle Scholar
  2. Bochner BR (2001) Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res 11(7):1246–1255. PubMedPubMedCentralCrossRefGoogle Scholar
  3. Borucki MK, Peppin JD, White D, Loge F, Call DR (2003) Variation in biofilm formation among strains of Listeria monocytogenes. Appl Environ Microbiol 69(12):7336–7342. PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bren A, Park JO, Towbin BD et al (2016) Glucose becomes one of the worst carbon sources for E.coli on poor nitrogen sources due to suboptimal levels of cAMP. Sci Rep 6:2–11. CrossRefGoogle Scholar
  5. Buchanan RL, Gorris LGM, Hayman MM et al (2017) A review of Listeria monocytogenes: an update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control 75:1–13. CrossRefGoogle Scholar
  6. CDC (2012) Multistate outbreak of listeriosis linked to whole cantaloupes from Jensen Farms, Colorado| Listeria| CDC. Accessed 4 May 2018
  7. Chelvam KK, Yap KP, Chai LC, Thong KL (2015) Variable responses to carbon utilization between planktonic and biofilm cells of a human carrier strain of Salmonella enterica serovar Typhi. PLoS ONE 10(5):1–11. CrossRefGoogle Scholar
  8. Chong TM, Chen JW, See-Too WS et al (2017) Phenotypic and genomic survey on organic acid utilization profile of Pseudomonas mendocina strain S5.2, a vineyard soil isolate. AMB Express. PubMedPubMedCentralCrossRefGoogle Scholar
  9. Da Silva EP, De Martinis ECP (2013) Current knowledge and perspectives on biofilm formation: the case of Listeria monocytogenes. Appl Microbiol Biotechnol 97(3):957–968. PubMedCrossRefGoogle Scholar
  10. Doijad SP, Barbuddhe SB, Garg S et al (2015) Biofilm-forming abilities of listeria monocytogenes serotypes isolated from different sources. PLoS ONE 10(9):1–14. CrossRefGoogle Scholar
  11. Dutta V, Elhanafi D, Kathariou S (2013) Conservation and distribution of the benzalkonium chloride resistance cassette bcrABC in Listeria monocytogenes. Appl Environ Microbiol 79(19):6067–6074. PubMedPubMedCentralCrossRefGoogle Scholar
  12. Farrugia DN, Elbourne LDH, Hassan KA et al (2013) The complete genome and phenome of a community-acquired Acinetobacter baumannii. PLoS ONE 8(3):e58628. PubMedPubMedCentralCrossRefGoogle Scholar
  13. Gandhi M, Chikindas ML (2007) Listeria: a foodborne pathogen that knows how to survive. Int J Food Microbiol 113(1):1–15. PubMedCrossRefGoogle Scholar
  14. Giaouris EE, Simões MV (2018) Pathogenic biofilm formation in the food industry and alternative control strategies. In: Holban MA, Grumezescu MA (eds) Foodborne diseases: handbook of food bioengineering, 1st edn. Academic Press, Cambridge, Massachusetts, US, p 309–377. CrossRefGoogle Scholar
  15. Haber A, Friedman S, Lobel L et al (2017) l-Glutamine induces expression of Listeria monocytogenes virulence genes. PLoS Pathog 13(1):1–25. CrossRefGoogle Scholar
  16. Hain T, Chatterjee SS, Ghai R et al (2007) Pathogenomics of Listeria spp. Int J Med Microbiol 297(7–8):541–557. PubMedCrossRefGoogle Scholar
  17. Jamali H, Chai LC, Thong KL (2013) Detection and isolation of Listeria spp. and Listeria monocytogenes in ready-to-eat foods with various selective culture media. Food Control 32(1):19–24. CrossRefGoogle Scholar
  18. Jeyaletchumi P, Tunung R, Selina PM et al (2012) Assessment of Listeria monocytogenes in salad vegetables through kitchen simulation study. J Trop Agric Food Sci 40(1):55–62Google Scholar
  19. Kadam SR, den Besten HMW, van der Veen S et al (2013) Diversity assessment of Listeria monocytogenes biofilm formation: impact of growth condition, serotype and strain origin. Int J Food Microbiol 165(3):259–264. PubMedCrossRefGoogle Scholar
  20. Kalai Chelvam K, Chai LC, Thong KL (2014) Variations in motility and biofilm formation of Salmonella enterica serovar Typhi. Gut Pathogens 6(1):1–10. CrossRefGoogle Scholar
  21. Kathariou S (2002) Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J Food Prot 65(11):1811–1829. PubMedCrossRefGoogle Scholar
  22. Kuan CH, Wong WC, Pui CF et al (2013) Prevalence and quantification of Listeria monocytogenes in beef offal at retail level in Selangor, Malaysia. Brazil J Microbiol 44(4):1169–1172. CrossRefGoogle Scholar
  23. Lim SY, Yap KP, Thong KL (2016) Comparative genomics analyses revealed two virulent Listeria monocytogenes strains isolated from ready-to-eat food. Gut Pathogens 8(1):1–8. CrossRefGoogle Scholar
  24. Liu D (2006) Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J Med Microbiol 55(6):645–659. PubMedCrossRefGoogle Scholar
  25. Liu D (2008) Epidemiology. In: Liu D (ed) Handbook of Listeria monocytogenes. CRC Press, Florida, p 27–60CrossRefGoogle Scholar
  26. Lomonaco S, Nucera D, Filipello V (2015) The evolution and epidemiology of Listeria monocytogenes in Europe and the United States. Infect Genet Evol 35:172–183. PubMedCrossRefGoogle Scholar
  27. Marian MN, Sharifah Aminah SM, Zuraini MI et al (2012) MPN-PCR detection and antimicrobial resistance of Listeria monocytogenes isolated from raw and ready-to-eat foods in Malaysia. Food Control 28(2):309–314. CrossRefGoogle Scholar
  28. Mertins S, Joseph B, Goetz M et al (2007) Interference of components of the phosphoenolpyruvate phosphotransferase system with the central virulence gene regulator PrfA of Listeria monocytogenes. J Bacteriol 189(2):473–490. PubMedCrossRefGoogle Scholar
  29. Møretrø T, Schirmer BCT, Heir E et al (2017) Tolerance to quaternary ammonium compound disinfectants may enhance growth of Listeria monocytogenes in the food industry. Int J Food Microbiol 241:215–224. PubMedCrossRefGoogle Scholar
  30. Orsi RH, de Bakker HC, Wiedmann M (2011) Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol 301(2):79–96. PubMedCrossRefGoogle Scholar
  31. O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54(1):49–79PubMedCrossRefGoogle Scholar
  32. Ponniah J, Robin T, Paie MS et al (2010) Listeria monocytogenes in raw salad vegetables sold at retail level in Malaysia. Food Control 21(5):774–778. CrossRefGoogle Scholar
  33. Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M (2000) A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40(2):175–179. PubMedCrossRefGoogle Scholar
  34. Tang JYH, Carlson J, Mohamad Ghazali F et al (2010) Phenotypic MicroArray (PM) profiles (carbon sources and sensitivity to osmolytes and pH) of Campylobacter jejuni ATCC 33560 in response to temperature. Int Food Res J 17(4):837–844. CrossRefGoogle Scholar
  35. Tsai H, Hodgson DA (2003) Development of a synthetic minimal medium for Listeria monocytogenes. Appl Environ Microbiol 69(11):6943–6945. PubMedPubMedCentralCrossRefGoogle Scholar
  36. Wong WC, Pui CF, Chai LC et al (2011) Biosafety assessment of Listeria monocytogenes in vegetarian burger patties in Malaysia. Int Food Res J 18(1):459–463Google Scholar
  37. Zhou Q, Feng X, Zhang Q et al (2012) Carbon catabolite control is important for Listeria monocytogenes biofilm formation in response to nutrient availability. Curr Microbiol 65(1):35–43. PubMedCrossRefGoogle Scholar

Copyright information

© Bundesamt für Verbraucherschutz und Lebensmittelsicherheit (BVL) 2018

Authors and Affiliations

  1. 1.Institute of Biological Sciences, Faculty of ScienceUniversity of MalayaKuala LumpurMalaysia

Personalised recommendations