Skip to main content
SpringerLink
Log in

Factors influencing adhesion of bacteria Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus and yeast Pichia membranifaciens to wooden surfaces

  • Original
  • Published:
Wood Science and Technology Aims and scope Submit manuscript

Abstract

The aim of this study was to assess the potential of bacteria Escherichia coli ATCC 35218, Pseudomonas aeruginosa ATCC 27853, Staphylococcus aureus ATCC 25923 and yeast Pichia membranifaciens ZIM 2417 to adhere to wooden surfaces such as poplar (Populus sp.), Norway spruce (Picea abies), European beech (Fagus sylvatica), beech coated with the commercial Belinka oil food contact and disinfectant P3-oxonia active 150, and investigate their survival on the beech wood surface under different relative humidities (RH; 65%, 75%, 85%, 98%) and temperatures (10 °C, 20 °C, 27 °C/37 °C). To extend the research goals, the scanning electron microscopy (SEM) analysis was also performed. The adhesion was determined by the number of colony-forming units per mm2 of sample (CFU/mm2). Results showed that all tested bacteria and yeast were able to adhere to the wooden surfaces, although differences were observed according to strains and type of wood. It was evident that number of adhered cells of S. aureus was lower on spruce (3.62 × 103 CFU/mm2) compared to poplar and beech (1.09 × 105 and 2.11 × 104 CFU/mm2, respectively). Furthermore, oil and disinfectant promoted the adhesion of P. aeruginosa (155.93 and 130.50%, respectively) on the beech surfaces, while they had a strong inhibitory effect on the other tested microorganisms E. coli (87.44 and 88.44%, respectively), S. aureus (91.24 and 96.80%, respectively) and P. membranifaciens (92.45 and 87.24%, respectively). These findings are consistent with SEM micrographs. The current data also indicated that relative humidity and temperature significantly affected the adhesion of tested bacteria and yeast. The highest degree of adhesion was observed at a relative humidity of 98% and temperature of 20 and 37 °C for bacteria, or 20 and 27 °C for yeast. Thus, the knowledge of how these microorganisms adhere to wooden surfaces and which factors affect this phenomenon proves to be of great importance in order to avoid their colonization.

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

  • Ak N, Cliver D, Kaspar C (1994) Decontamination of plastic and wooden cutting boards for kitchen use. J Food Prot 57(1):23–30. https://doi.org/10.4315/0362-028X-57.1.23

    Article  Google Scholar 

  • Aviat F, Gerhards C, Rodriguez-Jerez J, Michel V, Le Bayon I, Ismail R, Federighi M (2016) Microbial safety of wood in contact with food: a review. Comp Rev Food Sci Food Saf 15:491–505. https://doi.org/10.1111/1541-4337.12199

    Article  Google Scholar 

  • Balasubramanian D, Mathee K (2009) Comparative transcriptome analyses of Pseudomonas aeruginosa. Hum Genom 3(4):349–361. https://ncbi.nlm.nih.gov/pmc/articles/PMC2897818/

  • Bohinc K, Dražić G, Abram A, Jevšnik M, Jeršek B, Nipič D, Kurinčič M, Raspor P (2016) Metal surface characteristics dictate bacterial adhesion capacity. Int J Adhes Adhes 68:39–46. https://doi.org/10.1016/j.ijadhadh.2016.01.008

    Article  CAS  Google Scholar 

  • Bohinc K, Nipič D, Godič-Torkar K, Oder M, Dražić G, Raspor P (2012) Bacterial adhesion to glass surface: influence of surface roughness. In: 26th Conference of the European colloid and interface society 2–7 September 2012, Malmö & Lund, Sweden, 30

  • Burčová Z, Kreps F, Greifová M, Jablonský M, Ház A, Schmidt Š, Šurina I (2018) Antibacterial and antifungal activity of phytosterols and methyl dehydroabietate of Norway spruce bark extracts. J Biotechnol 282:18–24. https://doi.org/10.1016/j.jbiotec.2018.06.340

    Article  CAS  Google Scholar 

  • Cardamone C, Cirlincione F, Gaglio R, Puccio V, Daidone F, Sciortino S, Mancuso I, Scatassa ML (2020) Behavior of four main dairy pathogenic bacteria during manufacturing and ripening of pecorino siciliano cheese. J Food Qual Hazards Control 7(2020):27–35

    CAS  Google Scholar 

  • Cruciata M, Gaglio R, Scatassa ML, Sala G, Cardamone C, Palmeri M, Moschetti G, Mantia TL, Settanni L (2018) Formation and characterization of early bacterial biofilms on different wood typologies applied in dairy production. Appl Environ Microbiol 84:e02107–e2117

    Google Scholar 

  • Davies D, Chakrabarty A, Geesey G (1993) Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl Environ Microbiol 59(4):1181–1186.https://ncbi.nlm.nih.gov/pmc/articles/PMC202258/

  • Fengel D, Wegener G (1989) Wood: chemistry, ultrastructure, reactions. Walter de Gruyter, Berlin

    Google Scholar 

  • Filip S, Fink R, Oder M, Jevšnik M (2012) Hygienic acceptance of wood in food industry. Wood Sci Technol 46:657–665.https://link.springer.com/article/10.1007/s00226-011-0440-0

  • Fink R, Filip S, Oder M, Jevšnik M (2013) Wood in food industry: potential applications and its limitations. In: Mendez-Vilos A (ed) Microbial pathogens and strategies for combating them: science, technology and education, vol 4. Badajoz, Spain, Formatex Research Center, pp 188–194

    Google Scholar 

  • Frank JF (2001) Microbial attachment to food and food contact surfaces. Rev Adv Food Nutr Res 43:319–370

    Article  CAS  Google Scholar 

  • Gaglio R, Cruciata M, Di Gerlando R, Scatassa ML, Cardamone C, Mancuso I, Sardina MT, Moschetti G, Portolano B, Settanni L (2016) Microbial activation of wooden vats used for traditional cheese production and evolution of neoformed biofilms. Appl Environ Microbiol 82:585–595. https://doi.org/10.1128/AEM.02868-15

    Article  CAS  Google Scholar 

  • Gaglio R, Cruciata M, Scatassa ML, Tolone M, Mancuso I, Cardamone C, Corona O, Todaro M, Settanni L (2019) Influence of the early bacterial biofilms developed on vats made with seven wood types on PDO Vastedda della valle del Belìce cheese characteristics. Int J Food Microbiol 291:91–103

    Article  CAS  Google Scholar 

  • Galinari É, da Nóbrega J, de Andrade N, de Luces Fortes Ferreira C (2014) Microbiological aspects of the biofilm on wooden utensils used to make a Brazilian artisanal cheese. Braz J Microbiol 45(2):713–720

  • Gough N, Dodd C (1998) The survival and disinfection of Salmonella typhimurium on chopping board surfaces of wood and plastic. Food Control 9(6):363–368. https://doi.org/10.1016/S0956-7135(98)00127-3

    Article  Google Scholar 

  • Haman N, Morozova K, Tonon G, Scampicchio M, Ferrentino G (2019) Antimicrobial effect of Picea abies extracts on E. coli growth. Molecules 24:1–10.

  • Hedge A (2015) Survival of Escherichia coli, Pseudomona aeruginosa, Staphylococcus aureus on wood and plastic surfaces. J Microb Biochem Technol 7(4):210–212.

  • Jevšnik M, Ovca A, Raspor P (2017) A comparison of three different cleaning methods for reducing contaminants on contact surfaces: a preliminary study.Int J Sanit Eng Res 11:55–66.

  • Laireiter C, Schnabel T, Köck A, Stalzer P, Petutschnigg A, Oostingh G, Hell M (2013) Active anti-microbial effects of larch and pine wood on four bacterial strains. BioResources 9(1):273–281

    Article  Google Scholar 

  • Lee S, Lee H, Min H, Park E, Lee K, Ahn Y, Cho Y, Pyee J (2005) Antibacterial and antifungal activity of pinosylvin, a constituent of pine. Fitoterapia 76:258–260.

  • Liu N, Lefcourt A, Nou X, Shelton D, Zhang G, Lo Y (2013) Native microflora in fresh-cut produce processing plants and their potentials for biofilm formation. J Food Prot 76(5):827–832. https://doi.org/10.4315/0362-028X.JFP-12-433

    Article  CAS  Google Scholar 

  • Liu S, Lu H, Hu R, Shupe A, Lin L, Liang B (2012) A sustainable woody biomass biorefinery. Biotechnol Adv 30:785–810.https://ncbi.nlm.nih.gov/pubmed/22306164

  • Lortal S, Di Blasi A, Madec M, Pediliggieri C, Tuminello L, Tanguy G, Fauquant J, Lecuona Y, Campo P, Carpino S, Licitra G (2009) Tina wooden vat biofilm: A safe and highly efficient lactic acid bacteria delivering system in PDO Ragusano cheese making. Int J Food Microbiol 132:1–8.

  • Milling A, Kehr R, Wulf A, Smalla K (2005) Survival of bacteria on wood and plastic particles: dependence on wood species and environmental conditions. Holzforschung 59:72–81. https://doi.org/10.1515/HF.2005.012

    Article  CAS  Google Scholar 

  • Møretrø T, Langsrud S (2017) Residential bacteria on surfaces in the food industry and their implications for food safety and quality. Comp Rev Food Sci Food Saf 16:1022–1041. https://doi.org/10.1111/1541-4337.12283

    Article  CAS  Google Scholar 

  • Munir MT, Pailhories H, Eveillard M, Aviat F, Lepelletier D, Belloncle C, Federighi M (2019) Antimicrobial characteristics of untreated wood: towards a hygienic environment. Health 11:152–170

    Article  CAS  Google Scholar 

  • Onilude A, Igbinadolor R, Wakil S (2010) Effect of time and relative humidity on the microbial load and physical quality of cashew nuts (Anacardium occidentale L.) under storage. Afr J Microbiol Res 4(19):1939–1944

    Google Scholar 

  • Payette M, Work T, Drouin P, Koubaa A (2015) Efficacy of microwave irradiation for phytosanitation of wood packing materials. Ind Crop Prod 69:187–196. https://doi.org/10.1016/j.indcrop.2015.01.030

    Article  CAS  Google Scholar 

  • Plumed-Ferrer C, Väkeväinen K, Komulainen H, Rautiainen M, Smeds A, Raitanen J, Eklund P, Willför S, Alakomi H, Saarela M, von Wright A (2013) The antimicrobial effects of wood-associated polyphenols on food pathogens and spoilage organisms. Int J Food Microbiol 164:99–107.

  • Raspor P, Goranovic D (2008) Biotechnological applications of acetic acid bacteria. Crit Rev Biotechnol 28(2):101–124. https://doi.org/10.1080/07388550802046749

    Article  CAS  Google Scholar 

  • Raspor P, Jevšnik M (2016) Food supply chains vs. food supply nets. Emerging and traditional technologies for safe, healthy and quality food 9–32.https://link.springer.com/book/10.1007%2F978-3-319-24040-4

  • Rauha J, Remes S, Heinonen M, Hopia A, Kähkönen M, Kujala T, Pihlaja K, Vuorela H, Vuorela P (2000) Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. Int J Food Microbiol 56:3–12.

  • Regulation of European Parliament, Council of the European Union (2004) Commission regulation no. 1935/2004 of 27 October 2004 on materials and articles intended to come into contact with food and repealing directives 80/590/EEC and 89/109/EEC. Off J Eur Union 338:4–17.

  • Regulations (2012) Regulation (EU) No 528/2012 of the European Parliament and of the Council of 22 May 2012 concerning the making available on the market and use of biocidal products. Off J Eur Union 1–123

  • Sagripanti J, Bonifacino A (2000) Resistance of Pseudomonas aeruginosa to liquid disinfectants on contaminated surfaces before formation of biofilms. J AOAC Int 83(6):1415–1422.

  • Schönwälder A, Kehr R, Wulf A, Smalla K (2000) Antibakterielle Eigenschaften von Holz beachtenswert (Antibacterial properties of wood remarkable) (In German). Holz-Zbl 147:2037–2038

    Google Scholar 

  • Schönwälder A, Kehr R, Wulf A, Smalla K (2002) Wooden boards affecting the survival of bacteria? Holz Roh- Werkst 60:249–257

    Article  Google Scholar 

  • Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. LWT Food Sci Technol 43:573–583

    Article  Google Scholar 

  • Siroli L, Patrignani F, Serrazanetti D, Chiavari C, Benevelli M, Grazia L, Lanciotti R (2017) Survival of spoilage and pathogenic microorganisms on cardboard and plastic packaging materials. Front Microbiol 8:1–10.

  • Soumya A, Mohamed M, Fatimazahra B, Hassan L, Abdellah H, Fatima H, Saad I (2011) Study of microbial adhesion on some wood species: theoretical prediction. Microbiol 80:43–49.

  • Tomičić R, Raspor P (2017) Influence of growth conditions on adhesion of yeast Candida spp. and Pichia spp. to stainless steel surfaces. Food Microbiol 65:179–184. https://doi.org/10.1016/j.fm.2017.02.008

    Article  CAS  Google Scholar 

  • Tomičić R, Tomičić Z, Raspor P (2017) Adhesion of Candida spp. and Pichia spp. to wooden surfaces. Food Technol Biotechnol 55:138–142.

  • Vainio-Kaila T, Kyyhkynen A, Rautkari L, Siitonen A (2015) Antibacterial effects of extracts of Pinus sylvestris and Picea abies against Staphylococcus aureus, Enterococcus faecalis, Escherichia coli, and Streptococcus pneumoniae. BioResources 10:7763–7771. https://doi.org/10.15376/biores.10.4.7763-7771

    Article  CAS  Google Scholar 

  • Vainio-Kaila T, Zhang X, Hänninen T, Kyyhkynen A, Johansson LS, Willför S, Österberg M, Siitonen A, Rautkari L (2017) Antibacterial effects of wood structural components and extractives from Pinus sylvestris and Picea abies on methicillin-resistant Staphylococcus aureus and Escherichia coli O157:H7. BioResources 12:7601–7614

    CAS  Google Scholar 

  • Välimaa A, Honkalampi-Hämäläinen U, Pietarinen S, Willför S, Holmbom B, von Wright A (2007) Antimicrobial and cytotoxic knotwood extracts and related pure compounds and their effects on food-associated microorganisms. Int J Food Microbiol 115:235–243. https://doi.org/10.1016/j.ijfoodmicro.2006.10.031

    Article  CAS  Google Scholar 

  • Wyrwa J, Barska A (2017) Innovations in the food packaging market: active packaging. Eur Food Res Technol 243:1681–1692. https://doi.org/10.1007/s00217-017-2878-2)

    Article  CAS  Google Scholar 

  • Wu P, Huang J, Zheng Y, Yang Y, Zhang Y, He F, Chen H, Quan G, Yan J, Li T, Gao B (2019) Environmental occurrences, fate, and impacts of microplastics. Ecotoxicol Environ Saf 184:1–16. https://doi.org/10.1016/j.ecoenv.2019.109612

    Article  CAS  Google Scholar 

  • Zoz F, Iaconelli C, Lang E, Iddir H, Guyot S, Grandvalet C, Gervais P, Beney L (2016) Control of relative air humidity as a potential means to improve hygiene on surfaces: a preliminary approach with Listeria monocytogenes. PLoS ONE 11(2):1–14. https://doi.org/10.1371/journal.pone.0148418

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Ružica Tomičić thanks the Ministry of Education, Science and Technological Development Republic of Serbia (Project No. 451-03-68/2020-14/ 200134) and FEMS Research Grant (FEMS-RG-2016-0094) for financial support during study stay at Biotechnical faculty in Ljubljana and dr Neža Čadež for microbial strains.

Author information

Authors and Affiliations

  1. Faculty of Technology, University of Novi Sad, Bulevar cara Lazara 1, 21000, Novi Sad, Serbia

    Ružica Tomičić

  2. Institute of Food Technology, University of Novi Sad, Bulevar cara Lazara 1, 21000, Novi Sad, Serbia

    Zorica Tomičić

  3. Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, 1000, Ljubljana, Slovenia

    Nejc Thaler, Miha Humar & Peter Raspor

  4. Silvaprodukt d.o.o., Dolenjska cesta 42, 1000, Ljubljana, Slovenia

    Nejc Thaler

Authors
  1. Ružica Tomičić
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zorica Tomičić
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nejc Thaler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Miha Humar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter Raspor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter Raspor.

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

Tomičić, R., Tomičić, Z., Thaler, N. et al. Factors influencing adhesion of bacteria Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus and yeast Pichia membranifaciens to wooden surfaces. Wood Sci Technol 54, 1663–1676 (2020). https://doi.org/10.1007/s00226-020-01222-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00226-020-01222-0

Search

Navigation