Unraveling Microbial Biofilms of Importance for Food Microbiology
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Microb Ecol (2014) 68:35–46 DOI 10.1007/s00248-013-0347-4 MINIREVIEWS Unraveling Microbial Biofilms of Importance for Food Microbiology Lizziane Kretli Winkelströter & Fernanda Barbosa dos Reis Teixeira & Eliane Pereira Silva & Virgínia Farias Alves & Elaine Cristina Pereira De Martinis Received: 15 August 2013 /Accepted: 6 December 2013 /Published online: 27 December 2013 # Springer Science+Business Media New York 2013 Abstract The presence of biofilms is a relevant risk factors in Introduction the food industry due to the potential contamination of food products with pathogenic and spoilage microorganisms. The It is known that bacteria are remarkably capable of adjusting majority of bacteria are able to adhere and to form biofilms, their needs for survival in environments. Among the microbial where they can persist and survive for days to weeks or even characteristics enabling these adaptations one of the most longer, depending on the microorganism and the environmen- important is the ability of the microorganism to form biofilms, tal conditions. The biological cycle of biofilms includes sev- since it facilitates adaptation to harsh environmental eral developmental phases such as: initial attachment, matu- conditions. ration, maintenance, and dispersal. Bacteria in biofilms are In the last decades a substantial effort has been put forth to generally well protected against environmental stress, conse- improve our understanding on microbial biofilms, defined as quently, extremely difficult to eradicate and detect in food complex and well-organized biological communities embed- industry. In the present manuscript, some techniques and ded in a self-produced extracellular polymeric matrix that can compounds used to control and to prevent the biofilm forma- develop into moist surfaces, either biotic or abiotic [102, 180]. tion are presented and discussed. Moreover, a number of novel The presence of biofilms is common in food industry and techniques have been recently employed to detect and evalu- represents a concern because bacteria can adhere to almost ate bacteria attached to surfaces, including real-time polymer- anytypeofsurface,suchasplastic,metal,glass,soilparticles, ase chain reaction (PCR), DNA microarray and confocal laser wood and food products [7, 54]. The attachment of bacteria to scanning microscopy. Better knowledge on the architecture, food products or to product contact surfaces leads to economic physiology and molecular signaling in biofilms can contribute losses and also to a higher risk of occurrence of bacterial for preventing and controlling food-related spoilage and path- foodborne diseases. For example, contamination of equipment ogenic bacteria. The present study highlights basic and ap- with biofilms was a contributing factor to 59 % of food-borne plied concepts important for understanding the role of disease outbreaks investigated in France [120]. Bacterial in biofilms in bacterial survival, persistence and dissemination biofilms confer survival advantages to its members since they in food processing environments. are protected from environmental stress such as ultraviolet light, dehydration or treatment with antimicrobial and sanitizing agents, which makes their elimination a huge challenge [7, 37]. On the other hand, microbes in biofilms can L. K. Winkelströter : F. B. d. R. Teixeira : E. P. Silva : also be beneficial to food industry and may be used for E. C. P. De Martinis (*) biotechnological applications [41, 172]. For instance, it helps Faculdade de Ciências Farmacêuticas de Ribeirão Preto, the production of fermented food and in the waste treatment. Universidade de São Paulo (FCFRP-USP), Av. do Café s/n, 14040-903, Ribeirão Preto São Paulo, Brazil e-mail: [email protected] Biofilm in the Food Industry V. F. Al ve s Faculdade de Farmácia, Universidade Federal de Goiás (FF-UFG), Av. Universitária, esq. com 1ª Avenida, Setor Universitário, The attachment of bacteria with subsequent development of 74605-220 Goiânia, Goiás, Brazil biofilms on food industry surfaces has important consequences 36 L.K. Winkelströter et al. [169]. The occurrence of such structured microbial communi- Beneficial aspects of biofilms to the food industry should ties in food processing plants represents a reservoir of micro- also be mentioned and are related to biotechnological appli- organisms and serves as a potential source of contamination of cations. Biofilms are essential elements in the production of raw materials and processed products as they pass through fermented foods; for example, during the production of vine- various stages of food production operations. Moreover, the gar, the acetic acid bacteria are grown on wood chips and the presence of biofilms may lead to food spoilage, economical attachment of bacteria promote a more efficient conversion of losses, reduced shelf life of products or transmission of patho- substrate to acid [172]. Moreover, results from studies by gens [27, 82, 152, 169]. Demirci et al. [41] demonstrated that the production of ethanol The first report published on foodborne bacterial biofilm by Saccharomyces cerevisiae in biofilms presented advantage described the adhesive properties of Salmonella sp. [46], and in comparison to conventional fermentation since it had a since then, many bacteria have been identified to form biofilm higher productivity. According to Gamarra et al. [53], Asper- in the food industry premises, such as Listeria monocytogenes, gillus niger biofilms may be used for the commercial produc- Yersinia enterocolitica, Campylobacter jejuni, Staphylococcus tion of cellulases since biofilms formed on polyester cloth spp. and Escherichia coli O157:H7 [47, 161]. yielded 70 % more cellulase activity than freely suspended L. monocytogenes is commonly found in food processing mycelial culture. These enzymes are of importance due to environment, and it has been isolated from both meat and their potential industrial applications for the processing of dairy processing plants. This microorganism can adhere rap- food, textile, laundry, pulp and paper. idly and firmly to inert surfaces and may survive in the sessile Morikawa [125] highlighted good aspects related to form for a long period of time [32, 58, 71, 97, 129, 161, 176]. biofilm formation by B. subtilis and other bacilli due to For example, Unnerstad et al. [177] found the same clone of the control of infection caused by plant pathogens, the L. monocytogenes persisting in a dairy plant for 7 years and reduction of steel corrosion, and the exploitation of Miettinen et al. [121] demonstrated that isolates of novel compounds. Biofilm reactors were also applied L. monocytogenes PFGE type II had also survived in an ice to promote effective microbial growth for the treatment cream plant for at least 7 years. of sewage, industrial waste streams or contaminated Staphylococcus aureus is one of the most frequent food- groundwater [48]. It is very important to control harm- borne pathogens in the food industry [116, 152]. Some re- ful biofilm formation, but beneficial biofilms formed by searchers have observed the ability to adhere and form biofilm industrial bacteria may contribute for the development by Staphylococcus genus [116]. Rode et al. [152] studied of new biotechnological processes. biofilm formation by both food-related and clinical S. aureus strains grown under different stress conditions (temperature, sodium chloride, glucose and ethanol), and those authors Biofilm Formation observed that some ingredients, food such as sodium chloride and glucose, could promote biofilm formation by S. aureus. Biofilms can be defined as structured communities of bacteria, E. coli O157:H7 is known to produce exopolysaccharides which are adhered to each other and/or to surfaces or inter- (EPS) and to form biofilm on food-contact surfaces and faces and embedded in a self-produced exopolysaccharide equipment used in beef processing plant [20, 44]. Recently, matrix [38]. Their formation involves (1) initial attachment Mendonça et al. [117]alsodemonstratedthatE. coli O157:H7 of planktonic cells to the surface, (2) production of extracel- had the potential to form biofilm on different surfaces com- lular polimeric matrix (EPS), (3) microcolony formation and monly used by food industry while Dourou et al. [44]ob- secretion of chemical signals, (4) maturation of biofilm archi- served that E. coli O157:H7 attachment occurred not only at tecture and (5) dispersion of cells [62, 68, 123, 154]. However, temperatures of beef slaughter houses areas (15 °C), but also in this process of biofilm formation and detachment, some during cold storage (4 °C) temperatures, indicating more factors should be considered in more detail, as will be de- effective sanitation programs are necessary. scribed in sequence. Lactic acid bacteria (LAB) may cause biofilms and in this sense, it represents a concern for the food industry undesirable Biofilm Architecture changes in foods [87, 95]. One example is Lactobacillus curvatus, a nonstarter lactic acid bacterium that is capable of Biofilms formed by pathogenic bacteria, including Salmonella forming biofilm and produce an D-(−)-lactic acid, an isomer sp., L. monocytogenes, S. aureus, E. coli O157:H7, Bacillus responsible for the formation of calcium lactate crystals that cereus and Vibrio cholerae have been extensively studied on could lead to sensorial defects in cheeses [95]. Also, in situ biotic and abiotic surfaces [10, 17, 25, 164, 168, 179]. How- biofilm formation by Bacillus has been previously reported, ever, unattached