Production of O-desmethylangolensin, tetrahydrodaidzein, 6’-hydroxy-O-desmethylangolensin and 2-(4-hydroxyphenyl)-propionic acid in fermented soy beverage by lactic acid bacteria and Bifidobacterium strains

Highlights

• LAB and bifidobacteria produce daidzein and genistein in soy beverage.

• LAB and bifidobacteria are able to produce O-DMA, tetrahydrodaidzein and dihydrodaidzein.

• A putative isomer of dihydrodaidzein was produced by LAB and bifidobacteria.

• LAB and bifidobacteria produce 6-hydroxy-O-DMA and a high concentration of 2-(4-hydroxyphenyl)-propionic acid.

• LAB and bifidobacteria enrich soy drink with bioactive isoflavones with potential beneficial effects on human health.

Abstract

Isoflavones intake is associated with health benefits. The metabolism of isoflavones by bacteria plays a key role in their biotransformation. Therefore, commercial soy drink was fermented by 11 lactic acid bacteria (LAB) and 9 bifidobacteria strains. The majority of the strains showed deglycosylation of the isoflavone glycosides present in soy drink and appearance of the aglycones daidzein, genistein and glycitein. Moreover, we observed the further transformation of daidzein into O-desmethylangolensin (O-DMA) and tetrahydrodaidzein, alongside with dihydrodaidzein (DHD) and a putative isomer of DHD. On the other hand, genistein was transformed by nearly all strains into 6-hydroxy-O-desmethylangolensin (6-hydroxy-O-DMA), but no dihydrogenistein production was registered. A high concentration of 2-(4-hydroxyphenyl)-propionic acid was observed, suggesting the degradation of O-DMA and 6-hydroxy-O-DMA. The potential of LAB and Bifidobacterium strains to produce functional soy drink enriched with bioactive isoflavones is demonstrated in this work.

Introduction

Isoflavones are polyphenols biologically active, present in various plants, particularly in soybean germ (Vitale, Piazza, Melilli, Drago, & Salomone, 2013). They are classified as phytoestrogens since their structure resembles that of estrogen and they have a weak affinity for the estrogen receptor (Vaya & Tamir, 2004). These compounds have several biological activities, which confer them a beneficial potential on human health (Rietjens, Louisse, & Beekmann, 2017).

Isoflavones are usually found in nature in their glycosylated (daidzin, genistin, glycitin, puerarin) and/or methylated forms (formononetin, biochanin A). These glycosides are not absorbed at the intestine and must be hydrolysed to the aglycones daidzein, genistein and glycitein by the appropriate glycosidases and O-demethylases to become bioavailable and physiologically active (Gaya, Peirotén, & Landete, 2017). These transformations are carried out to a great extent by the intestinal microbiota.

The portion of aglycones that is not absorbed can be further transformed by the intestinal microbiota. In this way, daidzein can be transformed into dihydrodaidzein (DHD), O-desmethylangolensin (O-DMA) and/or equol, while genistein can originate dihydrogenistein (DHG), 6-hydroxy-O-DMA and/or 5-hydroxy-equol (Gaya, Peirotén, Álvarez, Medina, & Landete, 2018). These compounds produced by the intestinal microbiota are more bioavailable (Landete et al., 2016), and they have more estrogenic/antiestrogenic and antioxidant activities than their precursors (Morito et al., 2001), and have an effect in modulating hormone levels and the expression of estrogen receptors (Smeriglio et al., 2017, Mayo et al., 2019).

The plasma concentration of the isoflavone compounds resulting of intestinal microbiota metabolism is subjected to large inter-individual variability (van der Velpen et al., 2014), thus hindering the establishing of the effective intake doses of soy isoflavones. In this regard, the study of the bacteria responsible for the bioactivation of isoflavones could help to understand and overcome those inter-individual differences on isoflavone metabolism (Peirotén, Bravo, & Landete, 2019).

The ability to deglycosylate isoflavones has been extensively studied from soybean extracts, soy beverages, or from pure compounds as daidzin, genistin and glicitin (Raimondi et al., 2009, Rekha and Vijayalakshmi, 2011). Lactic acid bacteria (LAB) and Bifidobacterium strains producing β-glucosidases have great potential for the enrichment of bioactive isoflavones daidzein and genistein in soy beverage fermentation (Pyo et al., 2005, Raimondi et al., 2009). Nevertheless, large differences between strains in deglycosylation of glycosides were encountered in fermented soy beverages by LAB and Bifidobacterium strains (Delgado, Guadamuro, Flórez, Vázquez, & Mayo, 2019). However, the production of other metabolites derived from the metabolism of daidzein and genistein in soy beverage fermentation has not been described to date.

The demand of vegetarian alternatives for meat and dairy products is increasing, leading to the development of new soy-based products (Rizzo & Baroni, 2018). The new products based on soybeans must gather the sensory properties required by consumers, giving rise to the need of modifying soy drinks and foods containing soy extracts because of their peculiar taste (Granato, Ribeiro, Castro, & Masson, 2010). This has favored the development of soy-fermented foods containing additives to counteract soy drink strong flavours (Kaneko, Igarashi, & Aoyama, 2014). Another approach is the fermentation of soy drink, which besides of improving its sensory characteristics would increase its digestibility and the isoflavone bioavailability (Granato, Branco, Nazzaro, Cruz, & Faria, 2010).

In this work, we aimed to study the metabolism of isoflavones during the fermentation of soy drink by a selection of 20 LAB and bifidobacteria with biotechnological interest, many of which have shown the ability to metabolize different phytoestrogens or have other interesting traits (Table 1).