Fermentation of Date Pulp Residues Using Saccharomyces cerevisiae and Pichia kudriavzevii—Insights into Biological Activities, Phenolic and Volatile Compounds, Untargeted Metabolomics, and Carbohydrate Analysis Post In Vitro Digestion

Utilizing agricultural byproducts, such as date pulp residue (DPR), can contribute significantly towards achieving sustainable food production. This paper aimed to investigate the physicochemical properties of DPR and evaluate the health benefits of nonfermented and fermented DPR samples both pre- and post-digestion (bioaccessible portions). Additionally, it aimed to analyze the carbohydrates and untargeted metabolites in the bioaccessible portions. Fermentation of DPR by Saccharomyces cerevisiae and Pichia kudriavzevii resulted in an abundance of malic acid (over 2400 mg/100 g) and the identification of 42 volatiles, with different degrees of predominance observed in the samples. Twenty phenolics were determined by UPLC in fermented DPR, with (-)-epicatechin, tyrosol, and gallic acid being the most abundant. Bioaccessibility studies revealed that fermented DPR samples retained at least ~44% of α-glucosidase inhibition and exhibited improved α-amylase inhibition compared to nonfermented and undigested samples. In vitro cytotoxicity assays showed a more potent inhibitory effect of fermented DPR against MCF-7 and Caco2 cell lines (average inhibition of 55% and 74.4% for the two types of fermented samples) compared to nonfermented DPR. The untargeted metabolomics analysis identified C5-branched dibasic acid metabolism as the most prominent pathway, with four metabolites identified. Furthermore, the analysis of bioaccessible carbohydrate metabolites in the fermented DPR using LC-QTOF showed the presence of a group of phytochemicals, including three terpenoid metabolites.

[1]  Marcos dos Santos Lima,et al.  Effect of commercial yeasts (Saccharomyces cerevisiae) on fermentation metabolites, phenolic compounds, and bioaccessibility of Brazilian fermented oranges. , 2022, Food chemistry.

[2]  E. Çapanoğlu,et al.  Introduction to Novel Approaches in the Valorization of Agricultural Wastes and Their Applications. , 2022, Journal of agricultural and food chemistry.

[3]  M. Ayyash,et al.  In Vitro Characterization and Identification of Potential Probiotic Yeasts Isolated from Fermented Dairy and Non-Dairy Food Products , 2022, Journal of fungi.

[4]  A. Kamal-Eldin,et al.  Melanin is a plenteous bioactive phenolic compound in date fruits (Phoenix dactylifera L.) , 2022, Scientific Reports.

[5]  A. Tropea,et al.  Food Waste Valorization , 2022, Fermentation.

[6]  K. Ho,et al.  Extraction of phytochemicals with health benefit from Peperomia pellucida (L.) Kunth through liquid-liquid partitioning , 2022, Journal of Applied Research on Medicinal and Aromatic Plants.

[7]  M. Purugganan,et al.  Patterns of Volatile Diversity Yield Insights Into the Genetics and Biochemistry of the Date Palm Fruit Volatilome , 2022, Frontiers in Plant Science.

[8]  C. S. Riar,et al.  Effect of extraction methods and simulated in vitro gastrointestinal digestion on phenolic compound profile, bio-accessibility, and antioxidant activity of Meghalayan cherry (Prunus nepalensis) pomace extracts , 2022, LWT.

[9]  J. Simal-Gándara,et al.  Terpenes and terpenoids as main bioactive compounds of essential oils, their roles in human health and potential application as natural food preservatives , 2022, Food chemistry: X.

[10]  J. Lorenzo,et al.  Strategies to Increase the Value of Pomaces with Fermentation , 2021, Fermentation.

[11]  Ashok Pandey,et al.  Microbial engineering for the production of isobutanol: current status and future directions , 2021, Bioengineered.

[12]  D. G. Bortolini,et al.  Bioactivity and bioaccessibility of phenolic compounds from Brazilian fruit purees , 2021 .

[13]  M. Świeca,et al.  Influence of Phenolic-Food Matrix Interactions on In Vitro Bioaccessibility of Selected Phenolic Compounds and Nutrients Digestibility in Fortified White Bean Paste , 2021, Antioxidants.

[14]  W. Cao,et al.  Microbial Biosynthesis of L-Malic Acid and Related Metabolic Engineering Strategies: Advances and Prospects , 2021, Frontiers in Bioengineering and Biotechnology.

[15]  M. Taherzadeh,et al.  Date fruit processing waste and approaches to its valorization: A review. , 2021, Bioresource technology.

[16]  Yong Zhou,et al.  Plasma metabolites changes in male heroin addicts during acute and protracted withdrawal , 2021, Aging.

[17]  Z. Fang,et al.  Wine phenolic profile altered by yeast: Mechanisms and influences. , 2021, Comprehensive reviews in food science and food safety.

[18]  A. Kamal-Eldin,et al.  Biological activities of the bioaccessible compounds after in vitro digestion of low-fat Akawi cheese made from blends of bovine and camel milk. , 2021, Journal of dairy science.

[19]  A. Kamal-Eldin,et al.  Probiotic survival, biological functionality and untargeted metabolomics of the bioaccessible compounds in fermented camel and bovine milk after in vitro digestion. , 2021, Food chemistry.

[20]  B. Adhikari,et al.  Fermentation transforms the phenolic profiles and bioactivities of plant-based foods. , 2021, Biotechnology advances.

[21]  A. Vicente,et al.  Incorporation of olive pomace ingredients into yoghurts as a source of fibre and hydroxytyrosol: Antioxidant activity and stability throughout gastrointestinal digestion , 2021, Journal of Food Engineering.

[22]  A. Romano,et al.  Phenolic profile, antioxidant activity and enzyme inhibitory capacities of fruit and seed extracts from different Algerian cultivars of date (Phoenix dactylifera L.) were affected by in vitro simulated gastrointestinal digestion , 2021, South African Journal of Botany.

[23]  J. Teixeira,et al.  In Vitro Gastrointestinal Digestion Impact on the Bioaccessibility and Antioxidant Capacity of Bioactive Compounds from Tomato Flours Obtained after Conventional and Ohmic Heating Extraction , 2021, Foods.

[24]  V. Gupta,et al.  Valorization of fruits and vegetable wastes and by-products to produce natural pigments , 2021, Critical reviews in biotechnology.

[25]  G. Rodríguez-Gutiérrez,et al.  Valorization of date palm biodiversity: physico‐chemical composition, phenolic profile, antioxidant activity, and sensory evaluation of date pastes , 2021, Journal of Food Measurement and Characterization.

[26]  S. Bureau,et al.  Effect of storage conditions on ‘Deglet Nour’ date palm fruit organoleptic and nutritional quality , 2021, LWT.

[27]  S. Casal,et al.  Sugars and artificial sweeteners in soft drinks: A decade of evolution in Portugal , 2021 .

[28]  Y. Ogawa,et al.  Changes in bioactive compounds and antioxidant activity of plant-based foods by gastrointestinal digestion: a review , 2021, Critical reviews in food science and nutrition.

[29]  R. Rouf,et al.  Antioxidant properties and phenolic profiling by UPLC-QTOF-MS of Ajwah, Safawy and Sukkari cultivars of date palm , 2021, Biochemistry and biophysics reports.

[30]  H. Taher,et al.  Comparative study of lactic acid production from date pulp waste by batch and cyclic-mode dark fermentation. , 2020, Waste management.

[31]  S. Bhatia,et al.  Microbial Fermentation and Its Role in Quality Improvement of Fermented Foods , 2020 .

[32]  N. Narain,et al.  In vitro gastrointestinal digestion and probiotics fermentation impact on bioaccessbility of phenolics compounds and antioxidant capacity of some native and exotic fruit residues with potential antidiabetic effects. , 2020, Food Research International.

[33]  H. B. Rashmi,et al.  Phenolic acids from vegetables: A review on processing stability and health benefits. , 2020, Food research international.

[34]  Wenhai Xiao,et al.  Multi‐modular engineering of Saccharomyces cerevisiae for high‐titre production of tyrosol and salidroside , 2020, Microbial biotechnology.

[35]  Z. Ng,et al.  The antioxidant index and chemometric analysis of tannin, flavonoid, and total phenolic extracted from medicinal plant foods with the solvents of different polarities , 2020 .

[36]  A. Díaz,et al.  Influence of fermentation temperature and yeast type on the chemical and sensory profile of handcrafted beers. , 2020, Journal of the science of food and agriculture.

[37]  P. Show,et al.  Incorporating biowaste into circular bioeconomy: A critical review of current trend and scaling up feasibility , 2020 .

[38]  Héctor A. Ruiz,et al.  Spontaneously fermented traditional beverages as a source of bioactive compounds: an overview , 2020, Critical reviews in food science and nutrition.

[39]  Mahsa Majzoobi,et al.  Effects of Level and Particle Size of Date Fruit Press Cake on Batter Rheological Properties and Physical and Nutritional Properties of Cake , 2020 .

[40]  H. Alshwyeh.  Phenolic profiling and antibacterial potential of Saudi Arabian native date palm (Phoenix dactylifera) cultivars , 2020 .

[41]  D. Sun-Waterhouse,et al.  Fermentation-enabled wellness foods: A fresh perspective , 2019, Food Science and Human Wellness.

[42]  Hafiz M.N. Iqbal,et al.  Sustainable bioconversion of food waste into high-value products by immobilized enzymes to meet bio-economy challenges and opportunities - A review. , 2019, Food research international.

[43]  C. Varela,et al.  Volatile profile of reduced alcohol wines fermented with selected non-Saccharomyces yeasts under different aeration conditions. , 2019, Food microbiology.

[44]  M. Corredig,et al.  INFOGEST static in vitro simulation of gastrointestinal food digestion , 2019, Nature Protocols.

[45]  K. Khosravi‐Darani,et al.  Mycoprotein Production from Date Waste Using Fusarium venenatum in a Submerged Culture , 2019 .

[46]  Zhong Han,et al.  Sugar profile, volatile compounds, composition and antioxidant activity of Sukkari date palm fruit , 2018, Journal of Food Science and Technology.

[47]  D. Rossouw,et al.  Organic Acid Metabolism and the Impact of Fermentation Practices on Wine Acidity: A Review , 2018, South African Journal of Enology and Viticulture.

[48]  A. Kamal-Eldin,et al.  Reducing sugars, organic acids, size, color, and texture of 21 Emirati date fruit varieties ( Phoenix dactylifera , L.) , 2018, NFS Journal.

[49]  Weihong Min,et al.  Exploration of the molecular interactions between angiotensin-I-converting enzyme (ACE) and the inhibitory peptides derived from hazelnut (Corylus heterophylla Fisch.). , 2018, Food chemistry.

[50]  Maxim N. Artyomov,et al.  Electrophilic properties of itaconate and derivatives regulate the IκBζ–ATF3 inflammatory axis , 2018, Nature.

[51]  Edward T Chouchani,et al.  Itaconate is an anti-inflammatory metabolite that activates Nrf2 via alkylation of KEAP1 , 2018, Nature.

[52]  Sami Ghnimi,et al.  Classification of date fruit (Phoenix dactylifera, L.) based on chemometric analysis with multivariate approach , 2018, Journal of Food Measurement and Characterization.

[53]  L. V. Gonzaga,et al.  Effect of in vitro gastrointestinal digestion on the bioaccessibility of phenolic compounds, minerals, and antioxidant capacity of Mimosa scabrella Bentham honeydew honeys. , 2017, Food research international.

[54]  Yanyun Zhao,et al.  Functional properties, bioactive compounds, and in vitro gastrointestinal digestion study of dried fruit pomace powders as functional food ingredients , 2017 .

[55]  A. Pihlanto,et al.  Health benefits of fermented foods: microbiota and beyond. , 2017, Current opinion in biotechnology.

[56]  Shaoquan Liu,et al.  Modulation of the volatile and non-volatile profiles of coffee fermented with Yarrowia lipolytica: II. Roasted coffee , 2017 .

[57]  C. Cheok,et al.  Current trends of tropical fruit waste utilization , 2016, Critical reviews in food science and nutrition.

[58]  J. Tamang,et al.  Review: Diversity of Microorganisms in Global Fermented Foods and Beverages , 2016, Front. Microbiol..

[59]  Shaoquan Liu,et al.  Yeast and volatile evolution in cider co-fermentation with Saccharomyces cerevisiae and Williopsis saturnus , 2016, Annals of Microbiology.

[60]  L. Jakobek.  Interactions of polyphenols with carbohydrates, lipids and proteins. , 2015, Food chemistry.

[61]  M. Farag,et al.  Metabolomic fingerprints of 21 date palm fruit varieties from Egypt using UPLC/PDA/ESI-qTOF-MS and GC-MS analyzed by chemometrics. , 2014, Food research international.

[62]  J. Wendland,et al.  Major contribution of the Ehrlich pathway for 2-phenylethanol/rose flavor production in Ashbya gossypii. , 2014, FEMS yeast research.

[63]  A. Kader,et al.  Dates: postharvest science, processing technology and health benefits. , 2013 .

[64]  E. Çapanoğlu,et al.  A review on protein–phenolic interactions and associated changes , 2013 .

[65]  Maria Cekanova,et al.  Modulation of adipose tissue inflammation by bioactive food compounds. , 2013, The Journal of nutritional biochemistry.

[66]  A. Bahkali,et al.  Valorization of date palm (Phoenix dactylifera) fruit processing by-products and wastes using bioprocess technology - Review. , 2013, Saudi journal of biological sciences.

[67]  S. Guyot,et al.  Detailed polyphenol and tannin composition and its variability in Tunisian dates (Phoenix dactylifera L.) at different maturity stages. , 2013, Journal of agricultural and food chemistry.

[68]  Hammami Mohamed,et al.  Effects of the ripening stage on phenolic profile, phytochemical composition and antioxidant activity of date palm fruit. , 2012, Journal of agricultural and food chemistry.

[69]  Muthusamy Chandrasekaran,et al.  Valorization of Food Processing By-Products , 2012 .

[70]  C. Bertsch,et al.  Fruit cuticular waxes as a source of biologically active triterpenoids , 2012, Phytochemistry Reviews.

[71]  Geert Huys,et al.  Food fermentations: microorganisms with technological beneficial use. , 2012, International journal of food microbiology.

[72]  M. R. Bari,et al.  Optimizing endopectinase production from date pomace by Aspergillus niger PC5 using response surface methodology , 2010 .

[73]  H. Korpelainen,et al.  Biodiversity of date palms (Phoenix dactylifera L.) in Sudan: chemical, morphological and DNA polymorphisms of selected cultivars , 2009, Plant Genetic Resources.

[74]  S. Buxaderas,et al.  Different commercial yeast strains affecting the volatile and sensory profile of cava base wine. , 2008, International journal of food microbiology.

[75]  Jack T. Pronk,et al.  Malic Acid Production by Saccharomyces cerevisiae : Engineering of Pyruvate Carboxylation , Oxaloacetate Reduction , and Malate Export † , 2007 .

[76]  K. Verstrepen,et al.  Parameters Affecting Ethyl Ester Production by Saccharomyces cerevisiae during Fermentation , 2007, Applied and Environmental Microbiology.

[77]  F. Shahidi,et al.  Compositional and sensory characteristics of three native sun-dried date (Phoenix dactylifera L.) varieties grown in Oman. , 2005, Journal of agricultural and food chemistry.

[78]  S. Burt,et al.  Essential oils: their antibacterial properties and potential applications in foods--a review. , 2004, International journal of food microbiology.

[79]  K. Verstrepen,et al.  Expression Levels of the Yeast Alcohol Acetyltransferase Genes ATF1, Lg-ATF1, and ATF2 Control the Formation of a Broad Range of Volatile Esters , 2003, Applied and Environmental Microbiology.

[80]  J. Pech,et al.  Molecular and biochemical characteristics of a gene encoding an alcohol acyl-transferase involved in the generation of aroma volatile esters during melon ripening. , 2002, European journal of biochemistry.

[81]  Jun Kato,et al.  Inhibitory effects of triterpenoids and sterols on human immunodeficiency virus-1 reverse transcriptase , 2001, Lipids.

[82]  U. Ravid,et al.  Acetyl-coa: alcohol acetyltransferase activity and aroma formation in ripening melon fruits. , 2001, Journal of agricultural and food chemistry.

[83]  F. Shahidi,et al.  Phenolics in food and nutraceuticals , 1995 .

[84]  W H Barreveld,et al.  Date Palm Products , 1993 .

[85]  G. Flamini,et al.  Nutritional properties, aromatic compounds and in vitro antioxidant activity of ten date palm fruit (Phoenix dactylifera L.) varieties grown in Tunisia , 2022, Brazilian Journal of Pharmaceutical Sciences.

[86]  Qian Chen,et al.  l-glycine and l-glutamic acid protect Pediococcus pentosaceus R1 against oxidative damage induced by hydrogen peroxide. , 2022, Food microbiology.

[87]  The Date Palm Genome, Vol. 1: Phylogeny, Biodiversity and Mapping , 2021 .

[88]  M. Benichou,et al.  Evaluation of some nutritional quality criteria of seventeen Moroccan dates varieties and clones, fruits of date palm (Phoenix dactylifera L.). , 2021, Brazilian journal of biology = Revista brasleira de biologia.

[89]  R. Krueger.  Date Palm (Phoenix dactylifera L.) Biology and Utilization , 2021, The Date Palm Genome, Vol. 1.

[90]  H. Rohm,et al.  Fruit processing by-products as food ingredients , 2020 .

[91]  Z. Ng,et al.  Effects of different heat treatments on the antioxidant activity and ascorbic acid content of bitter melon, Momordica charantia , 2019, Brazilian Journal of Food Technology.

[92]  S. Patel,et al.  Fermentation of Food Wastes for Generation of Nutraceuticals and Supplements , 2017 .

[93]  K. Horikoshi,et al.  Enhanced production of isoamyl alcohol and isoamyl acetate by ubiquitination-deficient Saccharomyces cerevisiae mutants. , 2005, Cellular & molecular biology letters.