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How Fructophilic Lactic Acid Bacteria May Acín Albiac et al. Microb Cell Fact (2020) 19:182 https://doi.org/10.1186/s12934-020-01438-6 Microbial Cell Factories RESEARCH Open Access How fructophilic lactic acid bacteria may reduce the FODMAPs content in wheat-derived baked goods: a proof of concept Marta Acín Albiac1, Rafaella Di Cagno1* , Pasquale Filannino2*, Vincenzo Cantatore2 and Marco Gobbetti1 Abstract Background: FODMAPs (Fermentable oligosaccharides, disaccharides, monosaccharides, and polyols) intake is associated with the onset of irritable bowel syndrome symptoms. FODMAPs in wheat-derived baked goods may be reduced via bioprocessing by endogenous enzymes and/or microbial fermentation. Because of the inherent enzyme activities, bread made by baker’s yeast and sourdough may result in decreased levels of FODMAPs, whose values are, however, not enough low for people sensitive to FODMAPs. Results: Our study investigated the complementary capability of targeted commercial enzymes and metabolically strictly fructophilic lactic acid bacteria (FLAB) to hydrolyze fructans and deplete fructose during wheat dough fer- mentation. FLAB strains displayed higher fructose consumption rate compared to conventional sourdough lactic acid bacteria. Fructose metabolism by FLAB was faster than glucose. The catabolism of mannitol with the goal of its reuse by FLAB was also investigated. Under sourdough conditions, higher fructans breakdown occurred in FLAB inoculated doughs compared to conventional sourdough bacteria. Preliminary trials allowed selecting Apilactobacillus kunkeei B23I and Fructobacillus fructosus MBIII5 as starter candidates, which were successfully applied in synergy with com- mercial invertase for low FODMAPs baking. Conclusions: Results of this study clearly demonstrated the potential of selected strictly FLAB to strongly reduce FODMAPs in wheat dough, especially under liquid-dough and high oxygenation conditions. Keywords: FODMAP, IBS, Fructophilic lactic acid bacteria, Fructans, Wheat four, Bread Background FODMAPs are considered prebiotics contributing to Fermentable oligosaccharides, disaccharides, monosac- the healthy maintenance of intestinal microbiota, on charides, and polyols (FODMAPs) are heterogeneous the other side, FODMAPs intake is associated with the compounds, which, due to their chemical structure, are onset of irritable bowel syndrome (IBS) symptoms and poorly digestible and may exert a range of efects on other functional gut disorders [1, 2]. IBS is the most human gastrointestinal process. Fructans, galacto-oli- common gastrointestinal disorder worldwide, with a gosaccharides (GOS), lactose, fructose in excess of glu- prevalence estimated between 7 and 21% of the global cose, and sugar polyols (sorbitol and mannitol) are the population [2]. Triggering of IBS symptoms following main FODMAPs found in foods [1, 2]. Whether some consumption of FODMAPs is due to their poor absorp- tion at the small intestine level. Some FODMAPs are *Correspondence: [email protected]; [email protected] osmotically active, and their malabsorption draws 1 Faculty of Sciences and Technology, Libera Università di Bolzano, water into the intestinal and/or colonic lumen, caus- 39100 Bolzano, Italy ing diarrhea. Once reached the distal ileum and colon, 2 Department of Soil, Plant and Food Science, University of Bari Aldo Moro, 70126 Bari, Italy FODMAPs undergo the fermentation to short-chain © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Acín Albiac et al. Microb Cell Fact (2020) 19:182 Page 2 of 11 fatty acids and gases, causing bloating, abdominal pain, approaches targeting fructans-, fructose-, and mannitol- and fatulence [1, 2]. FODMAPs may also trigger the degrading enzymes/organisms [9]. manifestation of non-celiac wheat sensitivity [3, 4]. Our study aimed at investigating the complementary A low-FODMAPs diet may reduce symptoms associ- capability of targeted commercial enzymes and strictly ated to IBS or non-celiac wheat sensitivity [5, 6]. Being fructophilic lactic acid bacteria (FLAB) to fully degrade FODMAPs responsible for diversifed efects along the FODMAPs during wheat dough fermentation. As a newly gastrointestinal tract, a cutof value for each compound discovered bacterial group, FLAB are gaining increasing was defnable, which ranges from 0.15 to 1 g per serv- interest for their potential applications in food and phar- ing/meal for IBS patients [7]. Anyway, a diet therapy maceutical feld [12]. First, we screened strictly FLAB for based on the avoidance of FODMAPs restricts too their fructose consumption rates and mannitol degrad- much the food choices, eliminating staple foods, likely ing capabilities. Besides, we developed a novel protocol wheat derivatives and various vegetables, legumes and applied both under frm- and liquid-dough fermentation fruits. Under this dietary regimen, IBS patients should [13]. sufer for reduced intakes of fber, minerals, vitamins, and phytochemicals. In addition to the unbalanced Results nutritional status, the drastic reduction of FODMAPs Fructose consumption rate by FLAB during growth interferes with the intestinal microbiota and colonocyte into fructose‑glucose based medium metabolism [8]. Fructose consumption rate by FLAB strains, as well by Wheat-derived baked goods account for the major Lactiplantibacillus plantarum DC400 (formerly Lactoba- part of the daily consumed FODMAPs, mainly repre- cillus plantarum) and Fructilactobacillus sanfranciscensis sented by fructans and, to a lesser extent, GOS and fruc- SD8 (formerly Lactobacillus sanfranciscensis) (controls), tose, whereas mannitol is mostly present in sourdough was investigated during growth into Fructose Glucose bread [9]. Considering the risks associated to prolonged Yeast extract Peptone (FGYP) broth under aerobic con- implementation of low-FODMAP diet, various biotech- ditions. After 24 h at 30 °C, all the strains reached a cell nology strategies are under investigation for the manu- density of ca. 9‒9.5 Log CFU ml−1. Te fructose avail- facture of wheat-derived baked goods with reduced able in the medium (10 g L−1) was completely consumed FODMAPs content and suitable for IBS patients [10]. after 12–14 h by all FLAB, with the exception of Apilac- For instance, the use enzymes degrading fructans low- tobacillus kunkeei PLB29 and PFA3 (formerly Lactoba- ered the level of FODMAPs in bread. Whether humans cillus kunkeei), and Fructobacillus fructosus PFA23, for lack these enzymes, they are common in many plants which depletion was reached after 16 h. L. plantarum and microorganisms. Exoinulinases (EC 3.2.1.80) are DC400 and F. sanfranciscensis SD8 slowly metabolized specifc for the terminal linkages of inulin and release fructose; it was still detectable after 24 h. Kinetics of fructose, whereas endoinulinases (EC 3.2.1.7) have as tar- fructose consumption were modeled according to the get the internal β(2–1) glycosidic linkage, resulting into Gompertz equation as modifed by Zwietering et al. [14] oligosaccharides with a lower degree of polymerization. (Table 1). A. kunkeei strains showed μmax values ranging −1 −1 Using an exo-mechanism, invertase (β-fructofuranoside from 1.28 ± 0.18 to 3.51 ± 0.10 g L h , where λ values fructohydrolase EC 3.2.1.26) is able to catalyze the deg- ranged from 1.47 ± 0.17 to 8.32 ± 0.28 h. When Fructo. radation of inulin [10]. Apart from the enzyme used, the fructosus strains were used, μmax and λ ranged from −1 −1 hydrolysis of fructans correlates with the release of fruc- 0.96 ± 0.15 to 3.02 ± 0.15 g L h , and from 3.07 ± 0.25 tose, which is also within the FODMAP group, but only to 5.32 ± 0.32 h, respectively. As expected, the lowest when present in excess to glucose. Indeed, when fructose (P < 0.05) values of μmax were found with L. plantarum −1 −1 is present at the luminal level together with equimolar DC400 (0.28 ± 0.14 g L h ) and F. sanfranciscensis −1 −1 amounts of free glucose, the apical GLUT2 transporter SD8 (0.88 ± 0.08 g L h ). Tis latter had also the high- prevents the risk of fructose malabsorption [11]. Because est value of λ (13.76 ± 0.39 h). On the other side, glucose of the inherent enzyme activities, bread making by bak- metabolism by FLAB was slower than fructose (data not er’s yeast and sourdough may result in decreased levels of shown). FODMAPs, whose values are, however, not enough low for people sensitive to FODMAPs. Several causes might Mannitol consumption by FLAB into a mannitol‑based be responsible for this unsatisfactory result, likely the media short leavening/fermentation time, the release of fructose Aiming at selecting the best performing FLAB strains to from fructans, and the capability of hetero-fermentative metabolize mannitol, they were grown on Mannitol Yeast lactic acid bacteria to convert the fructose to mannitol extract Peptone (MYP) agar supplemented with CaCO 3, [10]. Terefore, low FODMAP baking needs dedicated containing mannitol as the only carbon source. Mannitol Acín Albiac et al. Microb Cell Fact (2020) 19:182 Page 3 of 11 Table 1 Kinetics parameters (μmax and λ)* of fructose consumption by bacterial strains Strain μmax λ Apilactobacillus kunkeei BIII59 1.98 0.12 fg 3.05 0.12 l ± ± A.
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