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Biofilm formation potential of Bacillus toyonensis and Pseudomonas aeruginosa on the stainless steel test surfaces in a model dairy batch system

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Abstract

Bacillus toyonensis (a Gram-positive bacterium) and Pseudomonas aeruginosa (a Gram-negative bacterium) isolated from the different surfaces of a dairy plant in our previous study were selected as the test bacteria for the present study. These two test bacteria were investigated in terms of their attachment on the stainless steel test surfaces in a model dairy batch system. After incubation at 5 °C and 20 °C for 6 h, 12 h, and 24 h, stainless steel plates were examined using cultural counts, profilometer, scanning electron microscopy (SEM), and fluorescent microscopy. Also, the test plates were subjected to a cleaning/disinfection procedure used in the dairy plant. Tests were employed before and after the cleaning/disinfection procedures. Cell wall characteristics and holding temperature were found to be significant for the attachment of the test bacteria to stainless steel test surfaces. In the study, the effect of the holding temperature varied depending on the type and characteristics of the bacteria. The adhesion ability of P. aeruginosa was higher than that of B. toyonensis. Increases in the holding temperature may increase the adhesion ability of the bacteria. Milk growth medium was found to be more successful in preventing the attachment ability of P. aeruginosa compared to B. toyonensis. This indicates that the chemical characteristic of the contact material may affect adhesion. The adhered bacterial cells were entirely removed by means of the cleaning/disinfection treatment. Therefore, the adhesion of bacterial cells could be explained as “initial phase of biofilm formation.” It can be concluded that the microorganism cell adhesion on the surface is followed by biofilm formation, and this situation lasts for many years. These results reveal the importance of controlling biofilm formation in dairy plants from the beginning.

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References

  • Bagge D, Hjelm M, Johansen C et al (2001) Shewanella putrefaciens. Appl Environ Microbiol 67:2319–2325. https://doi.org/10.1128/AEM.67.5.2319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baldwin RL (1986) Temperature dependence of the hydrophobic interaction in protein folding. Proc Natl Acad Sci U S A 83:8069–8072

    Article  CAS  Google Scholar 

  • Brown S, Santa Maria JP, Walker S (2013) Wall teichoic acids of Gram-positive bacteria. Annu Rev Microbiol 67:313–336. https://doi.org/10.1146/annurev-micro-092412-155620

    Article  CAS  PubMed  Google Scholar 

  • Chavant P, Martinie B, Meylheuc T et al (2002) Listeria monocytogenes LO28: surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl Environ Microbiol 728–737. https://doi.org/10.1128/AEM.68.2.728

  • Czerwonka G, Guzy A, Kałuz K, Dan M (2016) The role of Proteus mirabilis cell wall features in biofilm formation. 877–884. https://doi.org/10.1007/s00203-016-1249-x

  • Dewanti R, Wong ACL (1995) Influence of culture conditions on biofilm formation by Escherichia coli O157:H7. Int J Food Microbiol 26:147–164. https://doi.org/10.1016/0168-1605(94)00103-D

    Article  CAS  PubMed  Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol 15:167–193. https://doi.org/10.1128/CMR.15.2.167

    Article  CAS  Google Scholar 

  • Dunsmore DG (1981) Bacteriological control of food equipment by cleaning systems, 1 Detergent effects. Jounal Food Prot 44:15–20

  • Feil H, Bae YH, Feijen J, Kim SW (1993) Effect of comonomer hydrophilicity and ionization on the lower critical solution temperature of N-isopropylacrylamide copolymers. Macromolecules 26:2496–2500

    Article  CAS  Google Scholar 

  • Flint SH, Bremer PJ, Brooks JD (1997) Biofilms in dairy manufacturing plant-description, current concerns and methods of control. Biofouling J Bioadhesion Biofilm Res 11:81–97

    Article  CAS  Google Scholar 

  • Frank JF (2000) Control of biofilm in the food and beverage industry. In: Walker J, Surman S, Jass J (eds) Industrial biofouling. John Wiley & Sons Ltd., Chicester, N.Y., pp 205–224

    Google Scholar 

  • Frank JF (2001) Microbial attachment to food and food contact surfaces. Adv Food Nutr Res 43:319–370. https://doi.org/10.1016/S1043-4526(01)43008-7

    Article  CAS  PubMed  Google Scholar 

  • Giaouris E, Chorianopoulos N, Nychas GJE (2005) Effect of temperature, pH, and water activity on biofilm formation by Salmonella enterica Enteritidis PT4 on stainless steel surfaces as indicated by the bead vortexing method and conductance measurements. J Food Prot 68:2149–2154

    Article  CAS  Google Scholar 

  • Gibson H, Taylor JH, Hall KE, Holah JT (1999) Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms. J Appl Microbiol 87:41–48

  • Helke DM, Somers EB, Wong ACL (1993) Attachment of Listeria monocytogenes and Salmonella typhimurium to stainless steel and Buna-N in the presence of milk and individual milk components. J Food Prot 56:479–484

    Article  CAS  Google Scholar 

  • Hobbie JE, Daley RJ, Jasper S (1977) Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 1225–1228

  • Hunter AC, McCorquodale RM (1983) Evaluation of the direct epifluorescent filter technique for assessing the hygienic condition of milking equipment. J Dairy Sci 50:9–16

    CAS  Google Scholar 

  • Husmark U, Rönner U (1992) The influence of hydrophobic, electrostatic and morphologic properties on the adhesion of Bacillus spores. Biofouling 5

  • Jabra-Rizk MA, Falkler WA, Meiller TF (2004) Fungal biofilms and drug resistance. Emerg Infect Dis 10:14–19

    Article  CAS  Google Scholar 

  • Jeong DK, Frank JF (1994) Growth of Listeria monocytogenes at 21 °C in biofilms with micro-organism isolated from meat and dairy processing environments. LWT - Food Sci Technol 27:415–424

    Article  Google Scholar 

  • Jindal S, Anand S, Huang K et al (2016) Evaluation of modified stainless steel surfaces targeted to reduce biofilm formation by common milk sporeformers. J Dairy Sci 99:1–12. https://doi.org/10.3168/jds.2016-11395

    Article  CAS  Google Scholar 

  • Joseph B, Otta SK, Karunasagar I, Karunasagar I (2001) Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int J Food Microbiol 64:367–372. https://doi.org/10.1016/S0168-1605(00)00466-9

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Wei CI (2007) Biofilm formation by multidrug-resistant Salmonella enterica serotype Typhimurium phage Type DT104 and other pathogens. J Food Prot 70:22–29

    Article  CAS  Google Scholar 

  • Knight GC, Craven HM (2010) A model system for evaluating surface disinfection in dairy factory environments. Int J Food Microbiol 137:161–167. https://doi.org/10.1016/j.ijfoodmicro.2009.11.028

    Article  CAS  PubMed  Google Scholar 

  • Kumar CG, Anand SK (1998) Significance of microbial biofilms in food industry : a review. Int J Food Microbiol 42:9–27

    Article  CAS  Google Scholar 

  • Kumar CG, Singh RS (1994) Yersinia enterocolitica, as an emerging foodborne pathogen—a review. Indian J Dairy Sci 47:537–544

    Google Scholar 

  • Kütük Ayhan D, Temiz A, Asghari Sana F, Gümüşderelioğlu M (2019) Surface properties and exopolysaccharide production of surface-associated microorganisms isolated from a dairy plant. Ann Microbiol 69:895–907

    Article  Google Scholar 

  • Laird K, Armitage D, Phillips C (2012) Reduction of surface contamination and biofilms of Enterococcus sp. and Staphylococcus aureus using a citrus-based vapour. J Hosp Infect 80:61–66. https://doi.org/10.1016/j.jhin.2011.04.008

    Article  CAS  PubMed  Google Scholar 

  • Madigan MT, Martinko JM (2006) Brock biology of microorganisms, Eleventh E. Pearson Education, Inc., USA

  • Mafu AA, Roy D, Goulet J, Hagny P (1990) Attachment of Listeria monocytogenes to stainless steel, glass, polypropylene and rubber surfaces after short contact times. J Food Prot 53:742–746

    Article  CAS  Google Scholar 

  • Marques SC, Rezende JDGOS, Alves LADF et al (2007) Formation of biofilms by Staphylococcus aureus on stainless steel and glass surfaces and its resistance to some selected chemical sanitizers. Brazilian J Microbiol 38:538–543. https://doi.org/10.1590/S1517-83822007000300029

    Article  Google Scholar 

  • Mucchetti G (1995) Biological fouling and biofilm formation on membranes: fouling and cleaning in pressure driven membrane processes. Belgium, Brussels

    Google Scholar 

  • Özçelik Y, Costa G (2010) Comparison of the water jet and some traditional surface treatment method (Su jeti̇ ve bazı geleneksel yüzey i̇şleme yöntemlerinin karşılaştırılması; in Turkish) Madencilik 49:13–25

  • Pagedar A, Singh J, Batish VK (2010) Surface hydrophobicity, nutritional contents affect Staphylococcus aureus biofilms and temperature influences its survival in preformed biofilms. J Basic Microbiol 50:98–106. https://doi.org/10.1002/jobm.201000034

    Article  Google Scholar 

  • Poimenidou S, Belessi CA, Giaouris ED et al (2009) Listeria monocytogenes attachment to and detachment from stainless steel surfaces in a simulated dairy processing environment. Appl Environ Microbiol 75:7182–7188. https://doi.org/10.1128/AEM.01359-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers H, Perkins HR, Ward JB (1980) Microbial cell walls and membranes. Springer, Netherlands, Dordrecht

    Book  Google Scholar 

  • Rönner U, Husmark U, Henriksson A (1990) Adhesion of Bacillus spores in relation to hydrophobicity. J Appl Bacteriol 69:550–556

    Article  Google Scholar 

  • Rowe M, Gilmour A (1985) The present and future importance of psychrotrophic bacteria. Dairy Ind Int 50:14–29

    Google Scholar 

  • Ryu J, Beuchat LR (2005) Biofilm formation and sporulation by Bacillus cereus on a stainless steel surface and subsequent resistance of vegetative cells and spores to chlorine, chlorine dioxide, and a peroxyacetic acid – based sanitizer. J Food Prot 68:2614–2622

    Article  CAS  Google Scholar 

  • Sharma M, Anand SK (2002) Biofilms evaluation as an essential component of HACCP for food / dairy processing industry. A Case Food Control 13:469–477. https://doi.org/10.1016/S0956-7135(01)00068-8

    Article  CAS  Google Scholar 

  • Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2:1–16

    Article  Google Scholar 

  • Storgards E, Tapani K, Hartwall P, et al (2006) Microbial attachment and biofilm formation in brewery bottling plants. J Am Soc Brew Chem 64:8–15. https://doi.org/10.1094/ASBCJ-64-0008

  • Toncheva A, Paneva D, Maximova V et al (2012) Antibacterial fluoroquinolone antibiotic-containing fibrous materials from poly (L -lactide-co-D, L-lactide) prepared by electrospinning. Eur J Pharm Sci 47:642–651. https://doi.org/10.1016/j.ejps.2012.08.006

    Article  CAS  PubMed  Google Scholar 

  • Tortora JG, Funke RB, Case LC (1992) Microbiology. The Benjamin/Cummings Publishing Company Inc., California

    Google Scholar 

  • Vanhaecke E, Remon J, Moors M et al (1990) Kinetics of Pseudomonas aeruginosa adhesion to 304 and 316-L stainless steel: role of cell surface hydrophobicity. Appl Environ Microbiol 56:788–795

    Article  CAS  Google Scholar 

  • Vollmer W, Blanot D, De PMA (2008) Peptidoglycan Structure and Architecture 32:149–167. https://doi.org/10.1111/j.1574-6976.2007.00094.x

    Article  CAS  Google Scholar 

  • Wiencek KM, Klapes NA, Foegedingl PM, Carolina N (1990) Hydrophobicity of Bacillus and Clostridium spores. Appl Environ Microbiol 56:2600–2605

    Article  CAS  Google Scholar 

  • Wijman JGE, de Leeuw PP, Moezelaar R et al (2007) Air-liquid interface biofilms of Bacillus cereus : formation, sporulation, and dispersion. Appl Environ Microbiol 73:1481–1488. https://doi.org/10.1128/AEM.01781-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wirtanen G, Salo S, Helander IM (2001) Microbiological methods for testing disinfectant efficiency on Pseudomonas biofilm. Colloids Surfaces B Biointerfaces 20:37–50

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Hacettepe University Scientific Research Projects Coordination Unit (Project Codes: 014 D01 602 003 and FDK-2016–13096).

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  1. Department of Food Engineering, Hacettepe University, Beytepe, Ankara, Turkey

    Dilay Kütük & Ayhan Temiz

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  1. Dilay Kütük
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Correspondence to Dilay Kütük.

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Kütük, D., Temiz, A. Biofilm formation potential of Bacillus toyonensis and Pseudomonas aeruginosa on the stainless steel test surfaces in a model dairy batch system. Folia Microbiol 67, 405–417 (2022). https://doi.org/10.1007/s12223-021-00940-7

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