Impact of cooking and fermentation by lactic acid bacteria on phenolic profile of quinoa and buckwheat seeds
Graphical abstract
Introduction
In recent years, the exploitation of quinoa and buckwheat seeds in human nutrition is gaining a strong interest. This trend could be linked to the excellent nutrient profile and chemical composition of these pseudocereals (Alvarez-Jubete, Arendt, & Gallagher, 2010). To date, different studies have reported that common gluten-free (GF) foods are lower in nutritional quality when compared with gluten-containing counterparts (Padalino, Mastromatteo, Lecce, Cozzolino, and Del Nobile, 2013). Therefore, quinoa and buckwheat flours, that are naturally GF, could be valid alternative ingredients in GF diet for people suffering celiac disease and gluten-related disorders (Kupper, 2005).
Other than the nutritional quality and composition, these seeds are also rich in several bioactive compounds such as saponins, phytosterols, fagopyritols, and polyphenols (Wijngaard & Arendt, 2006; Alvarez-Jubete et al., 2010). In particular, polyphenols can be divided in five main classes, namely flavonoids, phenolic acids, lignans, stilbenes and other phenolics (including tyrosols and alkylphenols). These compounds possess different molecular weight and chemical structure and are widespread into vegetables as free and/or bound forms (González Aguilar, Blancas Benitez, & Sayago-Ayerdi, 2017). From a nutritional standpoint, bound phenolics are particularly interesting due to their ability to establish interactions with the food matrix, then being released into the small or large intestine, where they become available for bacterial microflora and promote an antioxidant environment (Rocchetti et al., 2018). Buckwheat is one of the best grain sources of polyphenols, being rich in flavonoids such as glycosidic forms of quercetin (a flavonol) followed by glycosidic forms of apigenin and luteolin (two of the main flavones) and phenolic acids (Alvarez-Jubete et al., 2010). Quinoa seeds are also abundant in phenolics such as flavonoids (i.e., glycosidic forms of the flavonols kaempferol and quercetin) and phenolic acids (Alvarez-Jubete et al., 2010; Rocchetti et al., 2017).
Buckwheat is usually eaten as a cooked grain, porridge or baked into pancakes in many countries (Moroni et al., 2012), while quinoa grains are commonly used to produce bread (Bender & Bender, 1999). Besides, alternative non-wheat grains and flours are commonly used to prepare fermented products featured by an improvement in both nutritional properties and shelf-life. For example, it has been shown that the fermentation of pseudocereal flours promoted by lactic acid bacteria (LAB) could improve both the sensory and baking quality, providing in this way food with attractive flavour and texture (Hur et al., 2014). Therefore, the improvement of fermentation technology on these matrices appears to be a very good opportunity to formulate novel functional and healthy foods (Coda, Di Cagno, Gobbetti, and Rizzello, 2014). The selection of adequate starter cultures for seeds' fermentation requires strains that are highly adapted to the cereal substrate (Sekwati-Monang, Valcheva, Ganzle, 2012). However, the choice of starter cultures has a critical impact on the final quality, with the characterization of LAB representing a crucial step in order to improve the final product from both nutritional and technological point of views (Coda et al., 2014). It is well known that fermentation by sourdough LAB is able to enrich the food matrix with organic acids, indirectly stimulating the hydrolysis of proteins through the production of endogenous proteases (Gobbetti et al. 2014). Therefore, the final fermented matrix is characterized by a better nutritional profile thanks to both the release of small peptides, amino acids, and bioactive compounds, and to the reduction of anti-nutritional factors (Gobbetti et al. 2014; Rizzello, Di Cagno, Monemurro & Gobbetti, 2016). To date, few studies have identified the specific contribution of cereal/pseudocereal enzymes and defined starter culture on the conversion of free and bound phenolics during fermentation processes (Gänzle, 2014). A presumable mechanism for fermentation-induced enhancement of phenolic and antioxidant activities in cereal grains is related to degrading enzymes present in secretes of fermenting microbes, which results in structural breakdown of cell wall matrix and increased accessibility of bound/conjugated phenolic compounds to enzymatic attack (Dordević, Siler-Marinković, & Dimitrijević-Branković, 2010). In this regard, LAB characterizing cereal grains are able to promote the enzymatic conversion of phenolic compounds, mainly by means of five class of enzymes, namely glycosyl hydrolases, esterases, tannin hydrolases, reductases and decarboxylases (Gänzle, 2014).
However, to the best of our knowledge, a comprehensive evaluation of the effect of fermentative activity promoted by autochthonous LAB on the entire phenolic and in vitro antioxidant profile of quinoa and buckwheat cooked seeds is still scarce (Carciochi, Galvan-D'Alessandro, Vandendriessche & Chollet, 2016). Therefore, in this work, a metabolomics-based approach (UHPLC-ESI-QTOF mass spectrometry) was used for the first time to investigate the impact of both cooking and microbial fermentation on the phenolic composition of quinoa and buckwheat seeds.
Section snippets
Samples
In this work, commercial quinoa (Chenopodium quinoa Willd., family: Chenopodiaceae) and buckwheat (Fagopyrum esculentum, family: Polygonaceae) grains (production year: 2016), washed thoroughly, were used. Quinoa samples were native of South-America, while buckwheat samples originated from Italy. Quinoa and buckwheat cooked seeds were used to formerly isolate autochthonous LAB, and then to fermentate the grains by the LAB therein isolated.
LAB isolation and identification
For each type of seed, 25 g of grains were added to
LAB isolation and characterization
The identification and intra-species differentiation allowed to group the 66 and 70 isolates gained from buckwheat and quinoa seeds respectively, within 25 strains and five species (Table 1): Pediococcus pentosaceus (14 strains of which 12 in Buckwheat) Lactobacillus paracasei (5 strains in Buckwheat), Leuconostoc mesenteroides (1 strain in Quinoa), Enterococcus mundtii (3 strains in Quinoa) and E. faecium (2 strains in Buckwheat). Our study has been focused on a total of 19 strains of P.
Conclusions
Two autochthonous LAB strains, namely P. pentosaceus and L. paracasei, were isolated from quinoa and buckwheat seeds and then used for the following fermentation process. An untargeted metabolomic approach based on UHPLC-ESI-QTOF mass spectrometry allowed to investigate the changes in the phenolic composition of these pseudocereals during microbial fermentation. The changes in antioxidant potential were evaluated by means of ferric reducing power (FRAP) and oxygen radical absorbance capacity
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Acknowledgements
GR was the recipient of a fellowship from the Doctoral School on the Agro-Food System (AgriSystem) of the Università Cattolica del Sacro Cuore (Piacenza, Italy). The authors thank the "Enrica e Romeo Invernizzi" Foundation (Milan, Italy) for kindly supporting the metabolomic facility.
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