Biofilms in plant-based fermented foods: Formation mechanisms, benefits and drawbacks on quality and safety, and functionalization strategies
Introduction
Plant-based diets have been widely recognized as crucial for achieving a healthy diet from sustainable food systems (Willett et al., 2019), but the short shelf life narrows down the accessibility. Fermentation appears as an effective approach to prolong storage and facilitate transportation to improve the food supply-chain (Kinnunen et al., 2020). Plant-based fermented foods, such as vinegar, kimchi, table olives, wine, and kombucha, are produced or preserved by the metabolic activities of microorganisms, which deliver unique flavors and high nutritions. During the fermentation process, formation of biofilms occurs often on the surface of the fermenting plant-based foods and related liquids, which is regarded as a form of inherent environmental adaptation from the planktonic state of microorganisms in harsh conditions, such as acidic pH, high osmotic pressure, and insufficient nutrition (Fig. 1) (Berlanga & Guerrero, 2016; Sadekuzzaman, Yang, Mizan, & Ha, 2015).
Traditionally, biofilms are a symbol of spoilage and significant efforts have been directed towards controlling and eliminating harmful biofilms. For instance, biofilms can lead to a secondary fermentation, step and further result in overoxidation (Yun, Kim, & Lee, 2019), turbidity (Zhang et al., 2018), texture collapse, off-flavor, and off-taste of the fermented foods (Perpetuini et al., 2018). Furthermore, biofilms can enhance the colonization of pathogenic and spoilage bacteria, contaminate the processing medium surface of the food production system, increase the resistance to antimicrobial agents, and ultimately have negative effects on food safety and human health. Decades of studies have been conducted on the prevention and disruption methods of harmful biofilms (Alvarez-Ordonez, Coughlan, Briandet, & Cotter, 2019; Galie, Garcia-Gutierrez, Miguelez, Villar, & Lombo, 2018; Toushik, Mizan, Hossain, & Ha, 2020), including surface modifications (Muro-Fraguas et al., 2020), cell-signal inhibition strategies (Das & Mehta, 2018), chemical treatments (Wang, Zhou, Kalchayanand, Harhay, & Wheeler, 2020), enzymatic disruption strategies (Sikdar & Elias, 2020), non-thermal plasma treatments (Gupta & Ayan, 2019), bacteriophages (Sofy, Abd El Haliem, Refaey, & Hmed, 2020), bacteriocins (Seo & Kang, 2020), biosurfactants (Satpute et al., 2016), and plant essential oils (Pejcic, Stojanovic-Radic, Gencic, Dimitrijevic, & Radulovic, 2020).
Although the formation of biofilms is conventionally associated with undesired consequences, growing evidence suggests that many biofilms possess protective functions, which can improve and modulate the metabolic activities of fermenting microorganisms (Chakravorty et al., 2016). In this review, we aim to provide a summary of biofilm formation in typical plant-based fermented foods to provide guidelines towards controlling the fermentation of the raw materials in order to improve product quality and safety. The general mechanisms and factors regulating biofilm formation in plant-based fermented foods are first discussed, followed by an overview of typical fermented foods and the corresponding biofilm formation processes for these foods with key regulating factors highlighted. In addition, both the negative and positive effects of biofilms on the fermented products are discussed, such as effects on flavor (Bastard et al., 2016; Fan, Huang, Chen, & Han, 2020; Grounta, Doulgeraki, Nychas, & Panagou, 2016), adhesive properties of fermentation microbes (Muhammad et al., 2020), and secreted substances including primary and secondary metabolites (Caggianiello, Kleerebezem, & Spano, 2016). In the last section, the potential applications of biofilms and future directions for development are discussed. The rational design and advanced development of biofilms can provide fermented foods with desirable characteristics regarding shelf-life, nutritional value, texture, taste, mouthfeel, flavor, and color, further leading to a sustainable manner in producing tasty health-promoting foods at low-cost and with high-efficiency. Advanced biofilm systems that are reproducibly accessible, culturable, and easy-to-manipulate, would also provide opportunities for dissecting the mechanisms of microbial community formation. As an experimentally programmable microbial ecosystem, biofilms potentially have a wide range of applications in biomaterials and biomedicine (Han et al., 2020).
Section snippets
Formation mechanism and regulating factors of biofilms in plant-based fermented foods
Biofilms are three-dimensional microbial communities that gather on the surface of fermented foods and are surrounded by exopolysaccharides (EPS), extracellular proteins, and extracellular DNA secreted by cells (Berlanga & Guerrero, 2016). Biofilm formation is generally recognized as a developmental process containing four distinct stages: attachment, proliferation, maturation, and dispersion (Fig. 1) (Gulati & Nobile, 2016). In this section, the mechanism of biofilm formation is discussed from
Representative microorganisms and biofilm formation in typical plant-based fermented foods
It is not rare for plant-based fermented foods to produce biofilms. In this section we will focus on the biofilm formation in typical plant-based fermented foods, which are derived from different categories of commodities. Factors affecting the formation of biofilms including (i) commodity profiles and nutrient sources, (ii) microbial physiology and microbial succession, (iii) fermentation conditions such as time-temperature effects, O2 contents, and pH conditions, and (iv) secondary
Negative effects on appearance and texture
Biofilms often occur on the surface of solid fermented foods or at the liquid-air interface for fermented sauces and drinks. During formation and maturation, the thickness of biofilms increases with the growth of the microorganism, which causes the appearance of “spots” or turbidity and further results in limited acceptance by consumers. For example, biofilms floating on top of beer can possess a slimy appearance or small dry patches, while spider web-like biofilms cause the occurrence of
Benefiting characteristic textures and flavors
Biofilm formation on the surface of solid fermented foods can maintain the food appearance, prevent excessive loss of water from the food, and avoid oxidative discoloration due to excessive contact between the food and oxygen. These combined effects have positive outcomes on the characteristic texture and the quality of fermented foods. For example, when sufu is covered with a biofilm, microorganisms decompose the nutrients in sufu to promote maturation and aging, while monascus can maintain
Protection, creative-utilization, and redesign of beneficial biofilms
Protecting and cultivating beneficial biofilms (such as starter biofilms) before, during, and after fermentation is crucial in controlling the food production process. For example, in order to mature the biofilms in sherry wine, it is necessary to agitate the wine to increase the dissolved oxygen, along with precisely controlling the ethanol content (15% v/v) and cellar temperature (22 °C). These approaches are also carried out to promote aging and to prevent the opportunistic proliferation of
Conclusion and outlooks
Biofilms are a special microbial construct produced by planktonic cells to resist extreme pH, high osmotic pressure, fermentation, and other environmental stressors. The influences of biofilms on fermented food quality, safety, and processability are double-edged, with benefits and drawbacks arising depending on the specific foods, biofilms, fermentation conditions, and other variables. For example, the physical thickness of a biofilm with a large quantity of EPS can promote a higher biological
Declaration of competing interest
The authors have declared no conflict of interest.
Acknowledgments
We would like to acknowledge Dr. Xiaoling Wang and Dr. Qixian Zhang for the helpful discussion. This work was supported by the National Global Talents Recruitment Program (J.G.), State Key Laboratory of Polymer Materials Engineering (J.G., Grant No. sklpme 2020-3-01), Double First Class University Plan (J.G.), Key Laboratory of Leather Chemistry and Engineering (J.G.), National Engineering Research Center of Clean Technology in Leather Industry (J.G.), China Postdoctoral Science Foundation
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Authors contributed equally.