Pf/Lm co-culture appeared to be more beneficial for Lm at 4ºC than at 20ºC. Shortening of the lag phase, which is rather long for Lm at low temperatures (Chan & Wiedmann, 2009) seems to be one of the mechanisms; the other presumably being the migration to the bottom
layers, later on. This late advantage would disappear when Pf cells get detached, as the biofilm reaches a dispersion or detachment stage (McDougald et al., 2012).
In the food chain context, refrigeration of foods and equipment represent a selective niche for psychrotrophs such as Pf and Lm (Valderrama & Cutter, 2013). There is therefore a need to know the conditions or factors that allow or enhance Lm growth, survival or cell transfer in the cold. Biofilms favor all that, and the presence of Pseudomonas favors higher levels of Lm in biofilms. Elimination of Pseudomonas and layered Pf and Lm-carrying biofilms are therefore adequate targets to reduce Lm prevalence and improve food safety.
Other saprophytic, psychrotrophic and good biofilm former bacteria different from Pseudomonas, which could form layered biofilms the strain of Pf used here. And maybe not all Lm strains are fit to dive into the biofilm‘s bottom layers; they may stay in more accessible locations, to the advantage of the food plant hygienist. In summary, cleaning procedures aimed at detaching the top biofilm layers occupied by Pseudomonas or a similar host, or penetration through them, could be a good strategy for Lm eradication.
A
CKNOWLEDGMENTSThe authors thank J.V. Martinez-Suarez for kindly providing persistent Listeria monocytogenes strains, CLSM services of the University Complutense for their skillful assistance, and the Spanish Ministry of Economy and Competition for funding project AGL2010-22212-C02-01.
R
EFERENCESAlmeida C, Azevedo NF, Santos S, Keevil CW, Vieira MJ. Discriminating Multi-Species Populations in Biofilms with Peptide Nucleic Acid Fluorescence In Situ Hybridization (PNA FISH). Plos One. 2011; 6(3).
Borucki MK, Peppin JD, White D, Loge F, Call DR. Variation in biofilm formation among strains of Listeria monocytogenes. Applied and Environmental Microbiology. 2003;
69(12):7336-42.
Bourion F, Cerf O. Disinfection efficacy against pure-culture and mixed-population biofilms of Listeria innocua and Pseudomonas aeruginosa on stainless steel, Teflon(R) and rubber. Sciences Des Aliments. 1996; 16(2):151-66.
Breen J, Barnes D, Ganguly R. Protective effect of Pseudomonas slime polysaccharide against Listeria monocytogenes. International Journal of Immunopharmacology. 1982;
4(4):262-268.
Buchanan RL, Bagi LK. Microbial competition: effect of Pseudomonas fluorescens on the growth of Listeria monocytogenes. Food Microbiology. 1999; 16(5):523-9.
Carpentier B, Chassaing D. Interactions in biofilms between Listeria monocytogenes and resident microorganisms from food industry premises. International Journal of Food Microbiology. 2004; 97(2):111-22.
Carpentier B, Cerf O. Review - Persistence of Listeria monocytogenes in food industry equipment and premises. International Journal of Food Microbiology. 2011; 145(1):1-8.
Chan YC, Wiedmann M. Physiology and Genetics of Listeria monocytogenes Survival and Growth at Cold Temperatures. Critical Reviews in Food Science and Nutrition. 2009;
49(3):237-53.
Chmielewski RAN, Frank JF. Biofilm Formation and Control in Food Processing Facilities.
Comprehensive reviews in food science and food safety. 2003; 2:22-32.
Combrouse T, Sadovskaya I, Faille C, Kol O, Guerardel Y, Midelet-Bourdin G.
Quantification of the extracellular matrix of the Listeria monocytogenes biofilms of different phylogenic lineages with optimization of culture conditions. Journal of Applied Microbiology. 2013; 114(4):1120-31.
Costerton, J.W. Toward a unified biofilm theory. In The Biofilm Primer (1st ed.); Heidelberg, CE, Ed.; Springer: Berlin, Germany. 2007.
Da Silva EP, Pereira De Martinis EC. Current knowledge and perspectives on biofilm formation: the case of Listeria monocytogenes. Applied Microbiology and Biotechnology.
2013; 97(3):957-68.
Elias S, Banin E. Multi-species biofilms: living with friendly neighbors. Fems Microbiology Reviews. 2012; 36(5):990-1004.
Farrag SA, Marth EH. Growth of Listeria monocytogenes in the presence of Pseudomonas fluorescens at 7-degrees-c or 13-degrees-c in skim milk. Journal of Food Protection.
1989; 52(12):852-5.
Fatemi P, Frank JF. Inactivation of Listeria monocytogenes/Pseudomonas biofilms by peracid sanitizers. Journal of Food Protection. 1999; 62(7):761-5.
Flemming H-C, Wingender J. The biofilm matrix. Nature Reviews Microbiology. 2010;
8(9):623-33.
Fratamico PM, Annous BA, Gunther IV NW. Biofilms in the food and beverage industries.
CRC Press, Woodhead Pub: Boca Raton, Oxford. 2009.
Gram L. Inhibitory effect against pathogenic and spoilage bacteria of Pseudomonas strains isolated from spoiled and fresh fish. Applied and Environmental Microbiology. 1993;
59(7):2197-203.
Habimana O, Guillier L, Kulakauskas S, Briandet R. Spatial competition with Lactococcus lactis in mixed-species continuous-flow biofilms inhibits Listeria monocytogenes growth.
Biofouling. 2011; 27(9):1065-72.
Harmsen M, Lappann M, Knochel S, Molin S. Role of Extracellular DNA during Biofilm Formation by Listeria monocytogenes. Applied and Environmental Microbiology. 2010;
76(7):2271-9.
Hassan AN, Birt DM, Frank JF. Behavior of Listeria monocytogenes in a Pseudomonas putida biofilm on a condensate-forming surface. J Food Prot. 2004; 67(2):322-7.
Hoben HJ, Somasegaran P. Comparison of the pour, spread, and drop plate methods for enumeration of Rhizobium spp in inoculants made from pre-sterilized peat. Applied and Environmental Microbiology. 1982; 44(5):1246-7
Huis in 't Veld JH. Microbial and biochemical spoilage of foods: an overview. International journal of food microbiology. 1996; 33(1):1-18.
Ibusquiza PS, Herrera JR, Vazquez-Sanchez D, Cabo ML. Adherence kinetics, resistance to benzalkonium chloride and microscopic analysis of mixed biofilms formed by Listeria monocytogenes and Pseudomonas putida. Food Control. 2012; 25(1):202-10.
Jaspe A, Oviedo P, Fernandez L, Palacios P, Sanjose C. Cooling raw-milk - change in the spoilage potential of contaminating Pseudomonas. Journal of Food Protection. 1995;
58(8):915-21.
Jeong DK, Frank JF. Growth of Listeria monocytogenes at 10-degrees-c in biofilms with microorganisms isolated from meat and dairy processing environments. Journal of Food Protection. 1994; 57(7):576-86.
Kaplan JB. Biofilm Dispersal: Mechanisms, Clinical Implications, and Potential Therapeutic Uses. Journal of Dental Research. 2010;89 (3):205-18.
Karunakaran E, Mukherjee J, Ramalingam B, Biggs CA. "Biofilmology": a multidisciplinary review of the study of microbial biofilms. Applied Microbiology and Biotechnology.
2011; 90(6):1869-81.
Kives J, Orgaz B, SanJose C. Polysaccharide differences between planktonic and biofilm-associated EPS from Pseudomonas fluorescens B52. Colloids and Surfaces B-Biointerfaces. 2006; 52(2):123-7.
Kjelleberg S, Givskov M. The Biofilm mode of life. Mechanisms and adaptations. Horizon Bioscience: Norfolk, UK. 2007
Liao CH, (2006). Pseudomonas related genera. In Food Spoilage Microorganisms. Blackburn CV, Ed.; CRC Press: Boca Raton, Fl. 2006: 507-540.
Lopez D, Vlamakis H, Kolter R. Biofilms. Cold Spring Harbor Perspectives in Biology.
2010; 2(7).
Lourenco A, Machado H, Brito L. Biofilms of Listeria monocytogenes produced at 12 degrees C either in Pure Culture or in Co-Culture with Pseudomonas aeruginosa showed Reduced Susceptibility to Sanitizers. Journal of Food Science. 2011; 76(2):M143-M8.
Lungu B, Ricke SC, Johnson MG. Growth, survival, proliferation and pathogenesis of Listeria monocytogenes under low oxygen or anaerobic conditions: A review. Anaerobe.
2009; 15(1-2):7-17.
Lungu B, Saldivar JC, Story R, Ricke SC, Johnson MG. The Combination of Energy-Dependent Internal Adaptation Mechanisms and External Factors Enables Listeria monocytogenes to Express a Strong Starvation Survival Response During Multiple-Nutrient Starvation. Foodborne Pathogens and Disease. 2010; 7(5):499-505.
Mann EE, Wozniak DJ. Pseudomonas biofilm matrix composition and niche biology. Fems Microbiology Reviews. 2012; 36(4):893-916.
Mariani C, Oulahal N, Chamba JF, Dubois-Brissonnet F, Notz E, Briandet R. Inhibition of Listeria monocytogenes by resident biofilms present on wooden shelves used for cheese ripening. Food Control. 2011; 22(8):1357-62.
McDougald D, Rice SA, Barraud N, Steinberg PD, Kjelleberg S. Should we stay or should we go: mechanisms and ecological consequences for biofilm dispersal. Nature Reviews Microbiology. 2012; 10(1):39-50.
Mellefont LA, Ross T. Effect of potassium lactate and a potassium lactate-sodium diacetate blend on Listeria monocytogenes growth in modified atmosphere packaged sliced ham.
Journal of Food Protection. 2007; 70(10):2297-305.
Mettler E, Carpentier B. Variations over time of microbial load and physicochemical properties of floor materials after cleaning in food industry premises. Journal of Food Protection. 1998; 61(1):57-65.
Moltz AG, Martin SE. Formation of biofilms by Listeria monocytogenes under various growth conditions. Journal of Food Protection. 2005; 68(1):92-7.
Moretro T, Langsrud S. Listeria monocytogenes: biofilm formation and persistence in food-processing environments. Biofilms. 2004; 1:107-121.
Morris BEL, Henneberger R, Huber H, Moissl-Eichinger C. Microbial syntrophy: interaction for the common good. Fems Microbiology Reviews. 2013; 37(3):384-406.
Nilsson L, Gram L, Huss HH. Growth control of Listeria monocytogenes on cold-smoked salmon using a competitive lactic acid bacteria flora. Journal of Food Protection. 1999;
62(4):336-42.
Nilsson RE, Ross T, Bowman JP. Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. International Journal of Food Microbiology. 2011; 150(1):14-24.
Orgaz B, Lobete MM, Puga CH, SanJose C. Effectiveness of Chitosan against Mature Biofilms Formed by Food Related Bacteria. Int J Mol Sci. 2011; 12(1):817-28.
Ortiz S, Lopez V, Villatoro D, Lopez P, Davila JC, Martinez-Suarez JV. A 3-Year Surveillance of the Genetic Diversity and Persistence of Listeria monocytogenes in an Iberian Pig Slaughterhouse and Processing Plant. Foodborne Pathogens and Disease.
2010; 7(10):1177-84.
Rendueles O, Ghigo J-M. Multi-species biofilms: how to avoid unfriendly neighbors. Fems Microbiology Reviews. 2012; 36(5):972-89.
Rieu A, Briandet R, Habimana O, Garmyn D, Guzzo J, Piveteau P. Listeria monocytogenes EGD-e biofilms: no mushrooms but a network of knitted chains. Appl Environ Microbiol.
2008; 74(14):4491-7.
Ryser ET, Marth EH. Listeria, listeriosis and food safety (3rd ed.). CRC Press: Boca Raton, FL. 2007.
Sasahara KC, Zottola EA. Biofilm formation by Listeria monocytogenes utilizes a primary colonizing microorganism in flowing systems. Journal of Food Protection. 1993;
56(12):1022-8.
Silby MW, Winstanley C, Godfrey SAC, Levy SB, Jackson RW. Pseudomonas genomes:
diverse and adaptable. Fems Microbiology Reviews. 2011; 35(4):652-80.
Simoes M, Simoes LC, Vieira MJ. Species association increases biofilm resistance to chemical and mechanical treatments. Water Research. 2009; 43(1):229-37.
Sorhaug T, Stepaniak L. Psychrotrophs and their enzymes in milk and dairy products: Quality aspects. Trends in Food Science & Technology. 1997; 8(2):35-41.
Srey S, Jahid IK, Ha S-D. Biofilm formation in food industries: A food safety concern. Food Control. 2013; 31(2):572-85.
Tirumalai PS, Prakash S. Expression of chitinase and chitin binding proteins (CBP's) by Listeria monocytogenes J0161 in biofilm and Co-culture broths. African Journal of Microbiology Research. 2011; 5(29):5188-93.
Valderrama WB, Cutter CN. An Ecological Perspective of Listeria monocytogenes Biofilms in Food Processing Facilities. Critical Reviews in Food Science and Nutrition. 2013;
53(8):801-17.
Verran J, Airey P, Packer A, Whitehead KA. Microbial retention on open food contact surfaces and implications for food contamination. In Advances in Applied Microbiology.
Laskin AI, Sariaslani S, Gadd GM, Eds.; 2008; 64:223-46.
Editor: Edmund C. Hambrick © 2014 Nova Science Publishers, Inc.
Chapter 7