In vitro evaluation of prebiotic activity, pathogen inhibition and enzymatic metabolism of intestinal bacteria in the presence of fructans extracted from agave: A comparison based on polymerization degree
Introduction
The prebiotic effect of fructans has been documented by some authors because they possess the ability to significantly modify intestinal microbiota (Krumbeck, Maldonado-Gomez, Ramer-Tait, & Hutkins, 2016). Fructans are molecules bonded by fructosyl linkages and generally they have a terminal glucose moiety. They may be present in approximately 15% of all flowering plants. Regarding their structure, five different types may be distinguished: inulin (β 2 → 1 linkage), levan (β 2 → 6 linkage) graminan (β 2 → 1 and β 2 → 6 linkages), inulin neoseries and levan neoseries (fructans possessing an internal glucose residue) (Peshev and Van den Ende, 2014, Ritsema and Smeekens, 2003). In Mexico, Agave is used as an important source of fructans. However, it has been reported that these plants contain more than one fructan structure. Agave contains branched graminan fructans, also known as “agavins”. These contain a complex mixture of fructans possessing different polymerization degrees (PD) (Mellado-Mojica and López, 2012, Praznik et al., 2013, Velázquez-Martínez et al., 2014). Because of their β linkages, fructans are not hydrolyzed by the human digestive enzymes and they are fermented only by some bacterial species found as intestinal colonic microbiota. This fermentation is beneficial to health as it may be translated into improved results from clinical blood tests, i.e. it regulates glucose and triglyceride levels, it enhances resistance against both intestinal and extra-intestinal pathogens, it modulates the immune response and it attenuates allergies. It has also been reported that fructans prevent body weight increases as it impacts on food intake and it regulates the satiety-related hormones (Delgado et al., 2010, Márquez-Aguirre et al., 2013, Santiago-García and López, 2014). Nevertheless, it was demonstrated that fructans possessing several PD display a different prebiotic activity (González-Avila et al., 2014, Mueller et al., 2016). Bacteria from the Lactobacillus and Bifidobacterium genera metabolize fructans exhibiting low PD, whereas bacteria residing at both proximal and distal colon metabolize those with high PD (Mueller et al., 2016, Van De Wiele et al., 2007). A recent study demonstrated that low PD fructans obtained from Agave tequilana prevent weight gain, hyperglycemia and fatty liver disease. Moreover, fructans showing several PD are involved in short-chain fatty acids biosynthesis, playing an important role on gastrointestinal health (Kleessen et al., 2001, Koenen et al., 2016). Among the approximately 300 described Agave species, nearly 75% are found on Mexican territory. However, less than 5% of these species are used during the production of alcoholic beverages and many others are not used for industrial purposes. The aim of this study was to evaluate in vitro the prebiotic activity displayed by those fructans obtained from seven agave species, which are characterized by different PD.
Section snippets
Agave fructans
In this study we used fructans extracted from Mexican agave. Two of them originated from Guanajuato (A. salmiana var. liso and A. salmiana var. chino), 3 of them from Veracruz (A. salmiana spp. crassipina, A. atrovirens and Agave spp.), and the last 2 from Jalisco (A. tequilana var. cenizo and A. tequilana spp.). Aqueous preparations of these extracts were used and their preparation was carried out as previously described (Lopez, Mancilla-Margalli, & Mendoza-Diaz, 2003). Briefly, fructans were
Bacterial growth in presence of different fructans
Eleven fructan samples extracted from 7 agave species were evaluated in this study (Table 1). They were obtained from Guanajuato, Veracruz and Jalisco and they showed different PD. Only two species (A. tequilana var. cenizo and A. salmiana spp. crassipina) contained fructans possessing low, intermediate and high PD. The other species contained fructans with a PD averaging between 8 and 12 fructan residues. Those samples were labeled as Native Agave Fructans (NAF).
Generally, in a regular MRS
Discussion
In this study, the effectiveness of probiotics and pathogens to carry out fructan metabolism was dependent on their PD and the agave species from which they were extracted. Moreover, Arrizon, Morel, Gschaedler, and Monsan (2010) reported that enzyme secretion contributes to the ability to metabolize fructans, in particular fructanhydrolases. It has also been demonstrated that fructans extracted from Agave tequilana Weber are metabolized more efficiently by exo-fructanhydrolases when compared to
Conclusions
Fructans extracted from A. salmiana spp. crassipina and A. tequilana var. cenizo were metabolized by L. paracasei. Therefore, fructans obtained from A. salmiana spp. crassipina, A. salmiana var. liso, A. atrovirens, A. tequilana spp. were metabolized by L. casei. Although previous works have shown that fructans may function as prebiotic against pathogens, these two major probiotics did not show an antibacterial effect. However, we observed changes regarding their enzyme-mediated metabolism and
Acknowledgments
The authors would like to thank the financial support granted by CONACYT (grant number 402440)and AGARED. We also thank MS Pamela Aldrete Herrera for the kind donation of fructan fractions needed to carry out this project.
References (37)
- et al.
Comparison of the water-soluble carbohydrate composition and fructan structures of Agave tequilana plants of different ages
Food Chemistry
(2010) - et al.
Immunomodulatory effects of fructans
Food Research International
(2010) - et al.
Technological characterization of lactic acid bacteria isolated from Armada cheese (a Spanish goats' milk cheese)
International Dairy Journal
(2003) - et al.
Industrial enzyme applications
Current Opinion in Biotechnology
(2002) - et al.
Degradation of cyanogenic glycosides by Lactobacillus plantarum strains from spontaneous cassava fermentation and other microorganisms
International Journal of Food Microbiology
(1999) - et al.
In vitro assessment of agave fructans (Agave salmiana) as prebiotics and immune system activators
International Journal of Biological Macromolecules
(2014) - et al.
Growth of selected probiotic strains with fructans from different sources relating to degree of polymerization and structure
Journal of Functional Foods
(2016) - et al.
Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: Bacteriocins and conjugated linoleic acid
International Journal of Food Microbiology
(2012) - et al.
Fructans: Prebiotics and immunomodulators
Journal of Functional Foods
(2014) - et al.
Structure of fructo-oligosaccharides from leaves and stem of Agave tequilana Weber, var. azul
Carbohydrate Research
(2013)
Fructans: Beneficial for plants and humans
Current Opinion in Plant Biology
An overview of the last advances in probiotic and prebiotic field
Lebensmittel-Wissenschaft und -Technologie- Food Science and Technology
Mechanisms of probiosis and prebiosis: Considerations for enhanced functional foods
Current Opinion in Biotechnology
Effects of blackberry juice on growth inhibition of foodborne pathogens and growth promotion of Lactobacillus
Food Control
Separación de una fracción de fructanos de Agave tequilana Weber variedad azul, con alto gp mediante filtración tangencial
In vitro prebiotic activity of fructans with different fructosyl linkage
International Journal of Probiotics and Prebiotics
Single disc versus multiple disc and plate dilution techniques for antibiotic sensitivity testing
Antibiotics Annual
Antipathogenic activity and preservative effect of levan (β-2,6-fructan), a multifunctional polysaccharide
International Journal of Food Science and Technology
Cited by (33)
Contributions of agaves to human health and nutrition
2023, Food BioscienceDevelopment of an in vitro distal gastric simulator to mimic the mechanical action of the human stomach
2022, Food Research InternationalCitation Excerpt :In addition, the disintegration increases as porcine gastric pepsin was added, demonstrating the importance of the enzymatic activity during digestion. Future work will focus on studying the release of nutrients in different foods using the IV-DGS in comparison with experiments performed using static simulators (Gamboa et al., 2018). It is worth mentioning that the IV-DGS mimicked only the distal part of the stomach where the stronger contractions with high amplitudes are presented in accordance with the in vivo studies reported by Schwizer et al. (2006).