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Review Article
Open Access Peer-reviewed

Lactic Acid Bacteria Isolated from Fruits: A Review on Methods for Evaluation of Probiotic Potential

Jéssica Pereira Barbosa, Dennia Pires de Amorim Trindade, Eliane Maurício Furtado Martins, Patrícia Amaral Souza Tette
Journal of Food and Nutrition Research. 2022, 10(10), 711-726. DOI: 10.12691/jfnr-10-10-9
Received September 14, 2022; Revised October 17, 2022; Accepted October 28, 2022

Abstract

This Lactic acid bacteria (LAB) are known to have many health-promoting properties, among them probiotic activity. Fruits and their by-products are colonized with certain types of these microorganisms on their surfaces and contain them as part of their composition. This review provides information about methods of isolation, characterization, and identification of LAB from fruits and their by-products, including methods of evaluating the probiotic potential of these microorganisms and development of probiotic products. The strategies reported in this review are useful to help researchers in their choice of methods, aimed at the future development of potentially probiotic fruit products with LAB isolates from fruits that address the needs of specific groups in the population that cannot obtain probiotics from dairy products.

1. Introduction

Mounting evidence suggests that a healthy diet including high fruit consumption plays an important role in preventing chronic diseases, increasing immunity, and decreasing the expression of inflammatory biomarkers 1, 2. The inclusion of a wide variety of fruits in the human diet can provide nutrients, bioactive compounds, vitamins, minerals, and fiber. In addition to their nutritional quality, fruits in general have intrinsic characteristics that positively influence the survival of some microorganisms, such as lactic acid bacteria (LAB), on their surfaces 3. LAB are a microbial group with the ability to withstand unfavorable conditions in the human body (for example, salivary enzymes, low pH, and pancreatic juice) and colonize intestinal epithelial cells. Many microorganisms belonging to this group are recognized for their probiotic potential 4, 5, 6. The consumption of probiotics in adequate amounts confers a health benefit on the host 7.

In the past few decades, the pattern of consumption of food products has changed considerably due to growing awareness of the need to include healthy foods in the diet. In this sense, the food industry has directed its attention toward the production of foods with functional properties that provide beneficial health effects in addition to their basic nutritional functions. Probiotics are an important component of this effort 8.

The vast majority of probiotic LAB used commercially in the food and pharmaceutical industries have their origins in the gastrointestinal tract of humans, but they can also be isolated from food such as dairy products 9, 10. However, fruits have been widely studied as a viable alternative source for the isolation of these microorganisms. In in vitro studies, these LAB isolates presented good results for future studies in vivo in order to verify their beneficial health effects 11, 12.

The techniques used to isolate and screen these microorganisms are diverse, with variable and debatable efficacy 8; moreover, due to the probiotic range of target functions and technological applications, the selection and evaluation of isolated LAB from fruits requires a multifaceted, comprehensive approach, ranging from morphological assessments to genetic analysis. When isolated from fruits, the autochthonous LAB also have inherent stability, which can contribute to their survival rate in food matrices with similar characteristics to those of the source matrices 13. Furthermore, the physicochemical characteristics of the fruits are similar to the conditions of the human gastrointestinal tract, such as the acidic environment 14. The characterization and identification of probiotic microorganisms isolated from fruits can provide several microbiological resources with improved capabilities for the manufacture of products with greater stability and production efficiency 15, 16.

The development of probiotic products derived from fruit-based food matrices is a viable alternative to diversify the intake of these microorganisms by the population. The consumption of probiotic dairy products can be limited by the growing popularity of vegetarianism, high number of individuals with lactose intolerance, individuals with cholesterol-restricted diets, and economic and social conditions 17. Thus, the isolation of LAB from fruits and their by-products, and the consequent development of non-dairy probiotic products through these microorganisms, presents a promising future 18. In this review, we have gathered comprehensive information for the selection of LAB from fruits in order to help researchers choose methods and selection criteria that favor the development of potentially probiotic fruit products.

2. Lactic Acid Bacteria Isolated from Fruits

Fruits have intrinsic characteristics that positively influence the survival of LAB. The naturally occurring intracellular spaces (pores) in their microarchitecture facilitate entry of bacteria into the plant tissue and survival therein. Furthermore, the cell walls of LAB naturally present in plants are more resistant to degradation, allowing bacterial adaptation to the environmental conditions of plant matrices, such as low humidity and the presence of antimicrobial compounds 16, 19, 20, 21.

Fruits are good sources of vitamins, minerals, sugars, and other phytonutrients important for microbial growth. In addition, the buffering capacity and presence of fructo-oligosaccharides, inulin, fiber, and polyphenols (tannins, phenols, and phytates) protect microorganisms from stomach acidity and provide substrates for multiplication in the intestine 16, 19, 20. The organic acids found in fruits lower the pH, constituting an important factor in the selection of microorganisms, since acidic conditions inhibit the survival of most pathogenic microorganisms that may colonize their surface 16. As each fruit has unique characteristics in terms of chemical composition, buffering capacity, competitive microbiota and natural antagonist compounds, the probiotic potential may vary from one to another 14, 16.

By-products generated during fruit processing can preserve many of the intrinsic fruit characteristics, as well as contributing to the survival of potentially probiotic LAB 12, 20. Since the processing of fruits to produce juices and pulp generates between 30% and 40% of all agro-industrial residues, it is extremely important to add value and economic interest to these residues, which require scientific and technological research to enable their use, since they are rich in bioactive compounds and can be good matrices for the growth of probiotic bacteria 22.

Studies emphasize a high level of diversity among the autochthonous LAB community in fruits and their by-products (Table 1). The functional characteristics of LAB isolated from fruits and their by-products allows them to be considered as probiotic candidates, with promising results obtained in in vitro viability tests 9, 14, 20, 23, 24.

3. Methods for Evaluation of Probiotic Potential

3.1. Isolation

The isolation of LAB in foods, that may be a source of these microorganisms, precedes sample preparation by suspension in a specialized solution, followed by serial dilution and plating on a solid culture medium for later selection of the different morphologies to be isolated. There are differences in the sample preparation process when it comes to the type of food matrix and quantity of the sample 25. Most of the tests that aim to isolate LAB from fruits and by-products use 0.9% saline as a suspension solution, 26, 27, 28 while other studies dissolve the samples in peptone water or salted water 3, 12, 29.

The use of a selective cultivation media for the sample preparation process is not very common in the literature. Culture media has nutrients among other substances that provide the necessary conditions for the inoculated microorganisms to multiply. Di Cagno et al. 30 performed pre-enrichment of the sample of each fruit analyzed in Man Rogosa and Sharpe broth (MRS), a standard medium commonly used and with wide application for the growth of most LAB genera, 31, 32 with incubation under shaking conditions.

From this, after the plating stage, colonies of different morphologies were isolated. This broth has glucose as a carbon source that serves as a substrate for bacteria, in addition to surfactants that facilitate the capture of nutrients by LAB 33. Tests that do not use enrichment broths such as saline water to dissolve the samples isolate a larger number of morphologically different colonies 34. Another medium used for LAB isolation is sterile water. Yang et al. 35 separately added pineapple and papaya residues to sterile water, which allowed the isolation of a higher number of colonies with distinct morphologies (n = 86) than reported in a study that used MRS in the sample preparation process 36.

Sample preparation with peptone water and saline water does not require incubation, but these diluents provide non-selective growth, allowing the growth of all bacteria in the sample, including non-LAB 37. In relation to peptone water, saline water and sterile water, MRS broth seems to be more efficient at restricting the growth of many colonies with different morphologies and consequently of possible Gram-negative bacteria. However, although commercial MRS broth was developed to allow excellent growth of Lactobacillus, most of these bacteria are still subjected to a process of self-inhibition, or even cell injury in this medium, which could hamper the isolation of some species of these genera in fruits 33.

The sample collection process, which precedes the preparation of dilutions, also does not differ greatly between studies. However, unlike most tests that do not clean the sample with some type of biocide, Azmi and Hashim 38 subjected. Malaysian fruits to different hygiene steps, using alcohol and sodium hypochlorite, isolating different types of LAB at the end of the experiment. LAB strains have low susceptibility to sodium hypochlorite, including L. plantarum and L. paracasei, probably due to the morphological characteristics of the cells and structural alteration of the cell wall, which impact on their permeability 39, 40. Therefore, the hygiene process of the samples does not seem to prevent the isolation of several LAB genera and species and could prevent the isolation of Gram-negative species.

Isolation of LAB colonies in food usually involves the use of a solid MRS culture medium. Due to differences in nutritional needs between the different species of LAB, this standard medium may not provide ideal growth conditions for all genera of these bacteria 41. In this sense, supplementing the agar with additional growth factors and nutrients may be an alternative for the more selective isolation of some LAB genera.

Variations exist in the supplementation of this culture medium between different LAB isolation tests in fruits. Rodríguez et al. 3 added sodium azide to MRS agar for the isolation of LAB in fresh tropical and subtropical fruits. Sodium azide inhibits some enzyme systems, such as catalase 42. Since LAB is characteristic of the absence of this system, 43 its growth is not affected by the presence of these compounds in the culture medium, which can be effective at eliminating many aerobic bacteria. Cycloheximide has also been added to MRS agar in some studies 3, 44 in order to inhibit fungi and yeasts, preventing possible contamination of the plates. Despite the possibility of adding supplements and some other nutrients to the culture medium, most LAB isolation tests from fruits are performed only with commercial MRS agar and still achieve promising results in the isolation of these bacteria. Therefore, the supplements in commercial culture medium may be dispensable for the isolation of LAB in fruits and their by-products.

LAB are microaerophilic and facultatively anaerobic, and the ideal temperature for their growth varies between 5 °C and 45 °C, according to the LAB species; however, they are generally mesophilic, as they have an optimum growth temperature between 30°C and 35°C 45. The optimum LAB temperature varies by genera. Enterococcus has an optimum temperature of 35–37°C; Fructobacillus, 30°C; Lactobacillus, 30–40°C, Leuconostoc, 20–30°C; and Pediococcus, 25-35°C 25, 46, 47, 48, 49. The culture incubation conditions in the analyzed studies differed in temperature and oxygen supply. Several authors incubated the cultures under anaerobic conditions, at 30 °C for 48 h, isolating genera such as Lactobacillus, Weisella, Enterococcus, and Pediococcus 3, 34, 50, while Verón et al. 51, under microaerophilic conditions, isolated bacteria of the genera Fructobacillus and Lactobacillus at 37°C for 48 h.

3.2. Phenotypic Characterization and Genetic Identification

LAB must be identified to the species level by combining phenotypic and genotypic tests. Phenotypic characterization includes morphological, physiological, and biochemical aspects. Morphological characteristics such as the shape, color, and texture of colonies can be observed directly by the naked eye and by microscopy, which allows visualization of cell shape, Gram staining, and the presence of flagella for motility. Physiological characteristics are associated with the conditions under which microorganisms multiply and survive, with different pH ranges, growth in various salt concentrations, and oxygen tolerance being tested. Biochemical characteristics can be tested by using biochemical reactions or metabolic activities of microorganisms, such as the type of lactic acid formed, carbon dioxide production from glucose and assays for metabolic products resulting from the activity of enzymes such as catalase 31, 52, 53, 54, 55.

For the characterization of LAB isolated from fruits, the phenotypic tests commonly performed are morphological analysis, Gram staining, and the catalase activity assay 3, 12, 34, 35, 36, 44, 51, 56, 57, 58. The motility test is also frequently performed, as it is a simple, rapid, and inexpensive methodology 12, 34, 36, 44, 51, 58. Additional phenotypic tests include growth at different temperatures, pH, and NaCl concentrations; production of gas from glucose; and the ability to acidify the culture medium 35, 51.

Phenotypic tests are useful to characterize a small number of isolates. The limitations must be considered, such as their low reproducibility, a result of the plasticity of bacterial growth, the methodological difficulties for large-scale applications, and their low discriminatory power, due to the low morphological diversity of LAB and their very similar nutritional and growth requirements. Still, bacterial isolates do not express all of their genes at the same time, because gene expression is related to environmental conditions 59, 60. Thus, to identify the species of LAB, genotypic tests are needed 53, 59, 60.

Sequence analysis of the 16S rRNA gene is the most often used method for genotypic identification. This method is based on the presence of specific variable regions of each bacterial species, with subsequent comparison to references from public domain databases, such as GenBank 3, 12, 34, 35, 36, 44, 51, 57, 61, 62, 63, 64. Garcia et al. 12 compared the 16S rRNA gene and Matrix-Assisted Laser Desorption Ionization–Time of Flight (MALDI-TOF MS) genetic sequencing techniques, reporting high congruence in the identification of LAB species, despite the discriminatory inability of the method to identify species of some strains of Lactobacillus. Despite being an effective alternative for bacterial identification in terms of cost and analytical duration, MALDI-TOF MS has low reproducibility and a limited reference database, requiring the use of molecular techniques 65.

Despite being frequently used in the literature, sequencing of the 16S rRNA gene may not be able to discriminate highly related species, especially those that are phenotypically and genotypically similar to one another, such as L. plantarum and L. paraplantarum; L. pentosus, L. casei, and L. paracasei; and Weisella cibaria and W. confuse 66, 67, 68. Thus, for differentiation and identification of these species, specific methodologies are needed, such as polyphasic taxonomy and complementary molecular techniques, for example, Repetitive Extragenic Palindromic-PCR (REP-PCR). The latter technique was used by Rodríguez et al. 3 to identify LAB isolated from fruits and flowers native from Argentina. This study contributed to the classification of a great diversity of species and strains of LAB in the analyzed samples. Techniques for evaluating robust taxonomic marker sequences, such as the pheS and recA genes, can also be used 53, 66, 67, 68 This method was used by Di Cagno et al. 36, 44 to identify the species W. cibaria and W. confusa, as well as Lactiplantibacillus plantarum, Lactiplantibacillus paraplantarum, and Lactiplantibacillus pentosus.

The DNA-DNA hybridization method, which determines the similarity between two DNA samples, is a reference to specify that an isolate belongs to a specific species, discriminating heterogeneous species and taxa. 53, 64, 69. This method was used by Yang, Tan, and Cai 35. However, it can be time-consuming and costly because it requires a large collection of reference microorganisms.

In strain identification, typing methods are used, such as DNA markers by hybridization type RAPD-PCR (Random Amplified Polymorphic DNA–Polymerase Chain Reaction, randomly amplified polymorphic DNA based on PCR). This technique was used by Di Cagno and colleagues between 2009 and 2011 34, 36, 44. Di Cagno 34 was unable to discriminate W. cibaria from W. confusa, which may be justified by the fact that this technique is not recommended for species identification. 53, 69, 70.

3.3. Probiotic Potential

The supposed probiotic effect of a certain food can be confirmed through the fulfillment of criteria/guidelines established by the Food and Agriculture Organization and World Health Organization (FAO/WHO). The development of these guidelines aimed to streamline the probiotic product evaluation process and ensure not only the safety of the microorganism but also the authenticity of the health benefit claims associated with each strain 7, 71. The strain designation of a probiotic microorganism is important, as different strains of the same species may have different health effects. The dose of ingestion is also a consideration that have to show an efficacy study to confer a benefit 72. In the selection process, the origin and safety of microorganisms must be considered, as well as their functional and technological aspects.

3.4. Safety Criteria

Among the recommended safety criteria are not having a history of association with intestinal diseases or disorders, not carrying transferable antibiotic resistance genes, not promoting intestinal mucus degradation, not translocating or inducing translocation of pathogenic microorganisms to intestinal extracellular sites, and not having pathogenicity factors such as hemolytic activity and gelatinase 7, 73, 74. The tests used to verify the safety of LAB isolated from fruit include the formation of biogenic amines, mucin degradation, hemolytic and gelatinase activity, and the evaluation of the antibiotic resistance pattern, the latter being the most frequent (Table 2) 3, 12, 20, 63, 75.

The mechanisms of antibiotic resistance are based on strategies that involve drug inactivation, preventing the drug from reaching its target, reducing susceptibility to the target 76. Probiotic bacteria have varied resistance to antimicrobials, due to their intrinsic characteristics or to resistance acquisition. Intrinsic resistance is based on the natural characteristics of the microorganism, such as the strain's physiology and structural peculiarities, with mechanisms related to antibiotic inactivation enzymes or mechanisms that serve as permeability barriers. The acquired resistance mechanisms, on the other hand, are generally obtained by mechanisms of genetic exchange that involve transformation with free DNA, transduction by means of bacteriophages, or conjugation involving plasmids, collectively called mechanisms of horizontal gene transfer (THG). These mechanisms represent a threat to human health because their plasmid-mediated resistance determinants can result in their expression and dissemination 77, 78, 79. Intrinsic resistance can confer survival advantages on potentially probiotic microorganisms, such as Lactobacillus, when compared with susceptible bacteria. Acquired resistance, on the other hand, represents the risk of being transferred to sensitive pathogens in the intestinal microbiome; therefore, the use of strains with this resistance mechanism for human consumption is not recommended 80.

As for virulence factors, the hemolytic activity exhibited by pathogenic microorganisms allows multiplication in the host, using binding proteins to capture and use iron. Since free iron is not available because it is linked to heme or to circulating proteins, such as transferrin or lactoferrin, the hemolytic activity to capture this ion is considered a pathogenic factor 81, 82. Although LAB do not require iron to multiply, some of them, such as certain species of the genera Enterococcus, may have hemolytic activity, being considered potentially virulent 83.

Biogenic amines are a group of low-molecular-weight nitrogen compounds produced by LAB, mainly through the decarboxylation of amino acids. They exist in most fermented foods, such as cheese, vegetables, yogurt, sausage, wine, and beer. Biogenic amines have an important metabolic role in living cells. However, excessive oral intake of these substances can cause nausea, headaches, skin rashes, and changes in blood pressure. Therefore, the control of biogenic amines is critical for the safety of fermented foods 84, 85.

The ability to degrade mucin is considered one of the valuable indicators of the potential for pathogenicity and local toxicity of bacteria. The mucus layer (mucin) that lines the surface of the gastrointestinal tract plays an important role in the mucosal barrier system. Any damage or disturbance to this mucin layer will compromise the defense function of the host's mucosa. Thus, a mucin degradation test is recommended as an important marker for the safety assessment of potentially probiotic LAB 86, 87.

Gelatinase is a protease that contribute for the pathogen virulence from the degradation of collagen. Enterococcus spp. are often associated with virulence due to the production of this enzyme. In a study conducted in an animal model, Enterococcus faecalis produced gelatinase, contributing to the pathogenesis of endocarditis 88. In an in vitro test, Enterococcus faecium, Lactococcus lactis, and Levilactobacillus brevis isolated from pomegranate did not show gelatinase activity 61.

Coagulases are proteins that activate prothrombin, which in turn converts fibrinogen into fibrin, leading to blood clotting and contributing to the development of pseudocapsules that promote the formation of abscesses and infection, as well as bacteremia and endocarditis. The ability of coagulase to stimulate the formation of clots in plasma is a defining property of Staphylococcus aureus - distinguishing it from coagulase-negative (less virulent) staphylococci -, although this enzyme is known not to be exclusive to this species 89. Therefore, verification of coagulase activity can be included as a safety aspect in LAB isolated from food 90.

Bacterial deoxyribonuclease (DNase) are enzymes (nucleases) that hydrolyze nucleic acids to produce oligonucleotides, with evidence reinforcing their role as virulence factors. More specifically, DNase may be involved in bacterial growth and biofilm maturation, as well as the ability of bacteria to neutralize and lead to the immune response of neutrophils 91. During microbial infection, neutrophils are recruited to the site of infection, releasing extracellular traps, which are DNA structures similar to a web, built from chromatin, proteases and antimicrobial peptides that capture and kill pathogenic bacteria. Microorganisms capable of producing DNASe degrade the DNA structure of the immune mechanism, dissipating the bactericidal activity of neutrophils. Pathogens can convert trap components degraded by nuclease, turning them into a counter trap that triggers the death of neutrophils 92, 93, 94.

3.5. Functionality Properties

Probiotic properties are specific to strain, condition and dose, and two strains belonging to same species do not have exactly the same probiotic potential. Strain specific criteria have been designed as in vitro assays for preliminary selection. The in vitro selection criteria related to functionality factors are proposed as predictors of the in vivo outcome of the new probiotics 7, 74, 95. The most used in vitro tests to predict the functionality of microorganisms isolated from fruits are resistance to gastric acid and bile acid, resistance to gastrointestinal enzymes and antimicrobial activity against potentially pathogenic bacteria 12, 20, 26, 27, 56, 61. Other tests performed include adherence to mucus and human epithelial cells, hydrophobicity of the cell surface, the ability to reduce pathogen adhesion to surfaces, and bile salt hydrolase activity 20, 26, 27.

A particular method used to test the resistance of LAB to the conditions of the gastrointestinal tract is the use of in vitro simulators, which simulate with certain precision the physiological conditions associated with gastrointestinal transit. These models, static or dynamic, reproduce the retention time, pH, bile salt concentration, and number of digestive enzymes. The systems can be controlled in real time and show the exact changes that appear after the specific action of each tested microorganism. Tests conducted according to dynamic models allow more precise control over experimental parameters, cost less, and take less time to perform. They do not require approval from an ethics committee and allow assessment of changes in the microbiota in different regions of the colon 96, 97. This methodology was recently applied to verify the survival of probiotic LAB inserted in meat and dairy products 98, 99 and has not yet been tested on fruit isolates.

The specific effect of a probiotic may need to have additional properties for a specific use. A potential probiotic strain can be tested, specifically for its effect. For example, Bifidobacterium animalis subsp. lactis was tested and considered a specific probiotic on modulation of innate immune function in the human host 100. As well as L. fermentum KC5b, qualified with a cholesterol-lowering capacity 101 and B. longum ATCC 15708 and L. acidophilus ATCC 4356 with antioxidant activity 102.

3.6. Technological Properties

Technological criteria are associated with tests of resistance, survival, and functionality during industrial processing and storage. Other desirable characteristics are the non-transmission of unpleasant flavors or changes in the texture of food 7, 73, 74.

The technological properties that have been tested on LAB isolated from fruits and their by-products include acidification capacity 3 and titratable acidity 56, tolerance to sodium chloride (NaCl) and the conditions of lyophilization and freezing 103, proteolytic and lipolytic activity 20, flavoring and texturing capabilities 3, 20, 56 and cinnamoyl esterase activity 3.

Acidification capacity is one of the most sought-after properties in LAB used in the food industry, since the production of lactic acid alters the taste of fermented foods and plays a bioconservative role by inhibiting the growth of pathogenic and food-spoilage bacteria 3, 104. The titratable acidity can be a useful assessment tool, since the levels and types of organic acids produced during the fermentation process depend on the species of LAB, the composition of the culture and the growing conditions 56.

LAB tolerance to sodium chloride and freezing or lyophilization capacity are also tests that verify its performance in industrialized products 104. NaCl is an essential ingredient used in the food industry to impart sensory characteristics and exercise a preservative role in food; however, a high concentration of NaCl can inhibit the growth of LAB 105. Although Lactobacillus has good tolerance to 2%–3% NaCl 106, growth in fermented vegetable isolates was verified under NaCl concentrations up to 6% 107. Albuquerque et al. 20 found tolerance of LAB isolated from fruit and by-products in the range of 1%–4% NaCl.

LAB exhibit different survival rates during freezing and frozen storage, depending on processing conditions. In a study with Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus, the decrease in acidification capacity during freezing and frozen storage was closely related to the operational conditions used during the fermentation, collection, isolation, freezing, and storage stages of the strains. This indicates that the production of lactic acid must be well managed, especially in an industrial environment. It was found that the higher the freezing rate and the lower the storage temperature, the better the bacterial resistance to freezing and frozen storage 108.

LAB are capable of producing numerous aromatic compounds. The production of diacetyl is the test most commonly performed on LAB isolated from fruits and has shown positive results 3, 20, 56. The production of ethyl esters, even in low quantities, also plays an important role in the development of fruity sensory characteristics in some foods, as verified by Rodríguez et al. 3.

The texturizing capacity of LAB isolated from fruits was observed by the synthesis of exopolysaccharides (EPS) and pectinase 3, 20. EPS plays an important role in the consistency and rheology of processed products, improving the texture and increasing the viscosity of finished products 104. Pectinases are hydrolytic enzymes that cleave pectic substances and that constitute a large proportion of plant tissues. This enzyme can also contribute to the control of fruit juice viscosity 109.

The ability of LAB to exercise proteolytic and lipolytic activities is also an important technological characteristic for the development of particular sensory aspects related to the texture and flavor of fermented foods 20, 104.

The activity of cinnamoyl esterases is an interesting criterion to evaluate in LAB from fruits. These enzymes degrade hydroxycinnamate esters and sugars present in the cell walls of plants, resulting in the presence of phenolic acids in their free form 110. The presence of this enzyme in initial cultures can enrich plant matrices in phenolic acids with high bioavailability for humans 111. Human tissues and biological fluids do not have esterases capable of hydrolyzing phenolic acids 110. In fruit isolates, Rodríguez et al. 3 demonstrated that the majority showed strong cinnamoyl esterase activity.

Studies related to the insertion of probiotics in food have advanced considerably in recent years, stimulated by a global understanding of the role of the intestinal microbiota in health and disease and also by the need to define effective strategies to shape a healthy microbiota. Thus, new studies seek to identify and demonstrate the probiotic potential of promising microbial species 72.

4. Development of Probiotic Products

It is important to determine the safety and functionality aspects of probiotic cultures, as well as aspects related to the production of probiotic foods 112. Analyses of the technological properties of LAB have contributed to the quality and stability of food products. The standards and acceptability of the final product, as well as the increased application possibilities of these microorganisms, depends on these tests 113.

Studies have associated the use of probiotic microorganisms in several non-dairy foods, such as meats, juices, jellies, dried fruits, vegetable- and grain-based products, confectionery products, and breakfast cereals. However, these incorporated microorganisms, in most cases, are isolated from dairy products or from the human microbiota, such as L. acidophilus NCIMB 8821 and Lactiplantibacillus plantarum NCIMB 8826, isolated from human saliva and Limosilactobacillus reuteri NCIMB 11951, isolated from human intestine 114, 115, 116. The technological characteristics of these common isolated cultures are widely studied in the development of products derived from fruits as vehicles of probiotic bacteria for human consumption. On the other hand, it is believed that the inclusion of cultures isolated from fruit matrices in products derived from matrices with similar characteristics to those of the source material may present better performance; however, these studies are still limited.

Some researchers have observed the probiotic potential of LAB isolated from fruits in products of similar matrix composition. Di Cagno et al. 28 isolated L. plantarum from raw tomatoes and used to ferment tomato juice. The final product presented elevated values of ascorbic acid, glutathione and total antioxidant activity. Fermentation of pineapple juice and avocado puree by autochthonous LAB also increase the antioxidant activity, nutritional value and shelf-stable 29, 50.

Lyophilized Lacticaseibacillus paracasei isolated from the by-products of graviola and Lactiplantibacillus plantarum isolated from Barbados cherry by-products showed satisfactory performance for incorporation into fruit juices considered as potentially probiotic products. Survival rates exceeded 75% after 4 months of frozen storage and 14 days of refrigeration. At the end of simulated in vitro digestion, in excess of 80% survival was observed 103.

The maintenance and viability of LAB in fermented and probiotic foods is a challenge in the industrial process. In this way, lyophilization and encapsulation of the culture provide protection to the cells and, therefore, increase the viability of the final product 117, 118. However, during the drying process, the cells withstand adverse environmental conditions, which can cause harmful effects on their survival. The main contributing factors to the loss of viability are osmotic shock and membrane damage, due to the formation of intracellular ice and recrystallization 119.

The microencapsulation of probiotic LAB has been restricted to cultures isolated from humans 117, 120, 121 This technique protects microbial cells during passage through the gastrointestinal tract, increases the chances of reaching the intestine in satisfactory quantities, and confers health benefits on consumers 122, 123. The encapsulation of probiotics using vegetable-based materials can perform well in food applications. Among the various encapsulating agents used are oils and vitamins from fruits and vegetables 124. Food matrices containing some of these substances could naturally assist in promoting some protection to the microorganisms present there. There is a positive relationship between encapsulation of plant materials and increased probiotic viability. Alginate isolated from pea protein-based and carrageenan-locust bean gum provided protection and survival of probiotics in the presence of simulated gastric fluid at 37°C. Thus, these agents can be good choices for the microencapsulation technique 125, 126, 127, 128.

In addition to the technological parameters, researchers have also evaluated the health effects of these microorganisms. In a randomized controlled experimental study, the effects of the probiotic Limosilactobacillus fermentum 296, derived from fruits, against cardiometabolic disorders induced by a high-fat diet were evaluated, suggesting that the microorganism, when supplemented for 4 weeks, improved the biochemical parameters and cardiovascular effects in rats 129. In another study, a new probiotic formulation of Limosilactobacillus fermentum (L. fermentum 139, L. fermentum 263, and L. fermentum 296), also isolated from fruit, was administered for 8 weeks to pups of male and female rats from mothers exposed to maternal dyslipidemia during pregnancy and lactation. These new probiotic cultures could improve lipid profiles and autonomic dysfunction in the tested pups 130, thus reaffirming the importance of inserting fruit isolates in non-dairy products for health-related benefits.

Studies indicate a great potential for commercialization of fruit juices due to the adequate delivery of probiotics; strong antimicrobial and antioxidant properties; and high content of vitamins, total phenols, amino acids, and exopolysaccharides. These products may have unique sensory characteristics, as well as properties beneficial to human health. All of these advantages are strictly associated with the use of a bacterial strain and the plant matrix 131.

In view of the diversity of fruit isolates identified and even registered, tested, and confirmed as potential probiotic cultures, there is a need to include them in fruit-based food matrices (Figure 1). These foods can offer several benefits to consumers’ health, especially for those that are limited in the consumption of dairy products.

5. Concluding Remarks and Future Prospects

The great diversity of LAB in fruits can be explored in many ways for the production of fermented and potentially probiotic products. The variety of techniques for selecting these microorganisms is considerable, and their effectiveness is variable. The research referenced in this review presented promising pathways for fruit isolates in safety, functional, and technological tests. Technological analyses are limited in their applicability to fruit-based food matrices. In vitro tests with LAB isolated from fruits presented promising probiotic potential. These tests are important for conducting future in vivo tests to demonstrate the effects on human health. It is notable that efforts are being made to isolate microorganisms from fruit and use them, in the near future, in the development of new probiotic products that address, in particular, specific groups that cannot obtain probiotics from dairy products. In conclusion, strategies and methods are recommended for the selection of fruit LAB to encourage further technological analysis in products with food matrices that have similar characteristics to the isolation matrices.

Acknowledgements

The authors thank the Graduate Program in Nutrition and Health (PPGNUT) and the School of Nutrition, Federal University of Goiás (Universidade Federal de Goiás–UFG) for the administrative and technical support.

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Published with license by Science and Education Publishing, Copyright © 2022 Jéssica Pereira Barbosa, Dennia Pires de Amorim Trindade, Eliane Maurício Furtado Martins and Patrícia Amaral Souza Tette

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Jéssica Pereira Barbosa, Dennia Pires de Amorim Trindade, Eliane Maurício Furtado Martins, Patrícia Amaral Souza Tette. Lactic Acid Bacteria Isolated from Fruits: A Review on Methods for Evaluation of Probiotic Potential. Journal of Food and Nutrition Research. Vol. 10, No. 10, 2022, pp 711-726. http://pubs.sciepub.com/jfnr/10/10/9
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Barbosa, Jéssica Pereira, et al. "Lactic Acid Bacteria Isolated from Fruits: A Review on Methods for Evaluation of Probiotic Potential." Journal of Food and Nutrition Research 10.10 (2022): 711-726.
APA Style
Barbosa, J. P. , Trindade, D. P. D. A. , Martins, E. M. F. , & Tette, P. A. S. (2022). Lactic Acid Bacteria Isolated from Fruits: A Review on Methods for Evaluation of Probiotic Potential. Journal of Food and Nutrition Research, 10(10), 711-726.
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Barbosa, Jéssica Pereira, Dennia Pires de Amorim Trindade, Eliane Maurício Furtado Martins, and Patrícia Amaral Souza Tette. "Lactic Acid Bacteria Isolated from Fruits: A Review on Methods for Evaluation of Probiotic Potential." Journal of Food and Nutrition Research 10, no. 10 (2022): 711-726.
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  • Figure 1. Schematic representation of most commonly methodologies used in the stages of isolation, identification and characterization of LAB from fruits and their by-products. Abbreviations: LAB (lactic acid bacteria)
  • Table 1. Genera and species, isolation techniques and identification of lactic acid bacteria from fruits
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