Bioactivity of food melanoidins is mediated by gut microbiota
Introduction
Melanoidins are end products of Maillard reaction (MR), which occurs among the amino group of an amino acid, protein, or vitamin and the carbonyl group of a reductive sugar or oxidized lipid (Rufián-Henares & Pastoriza, 2016). The MR is very common in foods since it happens during heating but also during storage at room temperature (Rufián-Henares et al., 2006, Tagliazucchi and Verzelloni, 2014). Melanoidins are therefore high molecular weight products responsible for the brown color of thermally treated foods like bread, coffee, cocoa, etc (Rufián-Henares & Delgado-Andrade, 2009). The detailed structure of melanoidins remains unknown due to the varied nature of the foods in which melanoidins are formed. Thus, in biscuits and bread, melanoidins are mainly composed of polysaccharides and proteins (melanoproteins), while in coffee and cocoa melanoidins are usually smaller and incorporate phenolic compounds such as chlorogenic acids or catechins (Morales, Somoza, & Fogliano, 2012).
Melanoidins make an important contribution to our diet: on average, around 10 g of melanoidins per day could be ingested (Fogliano and Morales, 2011, Pastoriza and Rufián-Henares, 2014). Therefore, knowing the possible benefits or risks of melanoidins to human health is important. Accordingly, many different biological effects have been attributed to melanoidins. They can behave as prebiotic (Helou et al., 2015, Jiménez-Zamora et al., 2015), they have an important antioxidant capacity (Delgado-Andrade and Morales, 2005, Carvalho et al., 2014, Pastoriza and Rufián-Henares, 2014, de la Cueva et al., 2017) and antimicrobial activity (Rufián-Henares & de la Cueva, 2009), and they can possess inhibitory activity against angiotensin I-converting enzyme (Rufián-Henares & Morales, 2007).
In the gut, dietary melanoidins escape gastrointestinal digestion (similarly to fiber) and reach the colon where they become substrates for the gut microbiota (Wang, Qian, & Yao, 2011). However, the potential bioactivity of melanoidins after being exposed to the gut microbiota has not been extensively studied. It has been proposed that the colon is the main region of the gut where melanoidins exert their effects since they escape digestion (Rufián-Henares & Pastoriza, 2015). However, fermentation of melanoidins by gut microbes and resulting production of short chain fatty acids (SCFAs) have not been yet deeply studied. SCFAs are the main microbial metabolites and have been attributed to several health effects. For example, decreasing the luminal pH is one of the most obvious effects of SCFAs release in the gut, which can hinder the growth of pathogenic bacteria. Butyrate is used as a substrate by the epithelial cells, and the three main SCFAs (acetate, propionate and butyrate) are important for the maintenance of the gut barrier (Ríos-Covián et al., 2016). In addition, all these SCFAs have a protective role in diet-induced obesity (Lin et al., 2012) since butyrate and propionate have been related to the production of gut hormones and therefore reduction of food intake (Ríos-Covián et al., 2016). SCFAs (mostly butyrate) could also have an important role in colorectal cancer protection via reducing inflammation and increasing cell apoptosis (Donohoe et al., 2014).
Taking all this information into account, the objective of this research was to investigate the fate of melanoidins during simulated gastrointestinal digestion and subsequent fermentation by human gut microbiota. We assessed how melanoidins shaped gut microbial community structure and its functionality (SCFAs production), and we measured the release of phenolic compounds and antioxidants as consequence of microbial metabolism.
Section snippets
Reagents
For the antioxidant assays, 2,4,6-Tri(2-pyridyl)-s-triazine (TPTZ), potassium persulfate, iron (III) chloride hexahydrate, 2,2-Diphenyl-1-picrylhydrazyl, 2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt, trolox ((±)-6-Hydroxy-2,5,7,8-tetramethylchromane-2-carboxylic acid), and methanol were purchased from Sigma-Aldrich (Germany). Short chain fatty acids and phenolic standards were from Sigma-Aldrich (Germany).
For the in vitro digestion and fermentation, the following
Results and discussion
Melanoidins are bioactive compounds generated during the thermal processing of foods (Rufián-Henares, Delgado-Andrade, & Morales, 2006) with bioactive effects potentially similar to those of fiber-enriched foods (Delgado-Andrade, Rufián-Henares, & Morales, 2007). Thus, in order to assess the bioactivity of food melanoidins and the effect of the gut microbiota over such bioactivity, ten melanoidins were isolated from different foods and subjected to an in vitro digestion-fermentation process
Conclusions
Melanoidins are an important part of our diet, reaching average amounts of 10 g/day. Here we have demonstrated that melanoidins can be used by gut microbes resulting in SCFAs production and also shaping their communities. Many melanoidins favored the growth of beneficial genera such as Bifidobacterium and Faecalibacterium. Gut microbes, by fermenting melanoidins, were able to release some phenolics initially linked to the melanoidin backbone, which in turn could increase phenolics absorption.
CRediT authorship contribution statement
Sergio Pérez-Burillo: Investigation, Methodology, Writing - original draft. Sumudu Rajakaruna: Investigation, Methodology, Formal analysis. Silvia Pastoriza: Conceptualization, Supervision, Writing - review & editing. Oleg Paliy: Formal analysis, Conceptualization, Funding acquisition, Writing - review & editing. José Ángel Rufián-Henares: Validation, Formal analysis, Writing - review & editing, Funding acquisition.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We are thankful to Denise Kramer for her assistance with high-throughput sequencing. This study was supported by the project AGL2014-53895-R from the Spanish Ministry of Economy and Competitiveness and by the European Regional Development Fund (FEDER) and by the National Science Foundation award DBI-1335772 to OP.
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