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      Recent Advances in the Understanding of Stress Resistance Mechanisms in Probiotics: Relevance for the Design of Functional Food Systems

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          Abstract

          In recent years, more and more scientific community, food producers, and food industry show increased interest in functional foods containing probiotics, which is a big challenge. The consumption of probiotics in the context of a balanced diet through the consumption of functional foods or through the intake of pharmaceutical preparations has proven to contribute to the improvement of human health, even contributing to the prevention of diseases. In order for probiotics to be considered suitable for consumption, they must contain a minimum concentration of viable cells, namely, at least 10 7 colony forming units of beneficial microbes per gram. Ensuring the viability of bacterial cells until the moment of consumption is the overriding priority of functional probiotic food manufacturers. Probiotic bacteria are subject to stress conditions not only during food manufacturing but also during gastrointestinal passage, which limit or even compromise their functionality. This paper first examines all the stressful conditions faced by probiotic cells in their production stages and related to the conditions present in the bioreactor fermentation and drying processes as well as factors related to the food matrix and storage. The stress situations faced by probiotic microorganisms during the gastrointestinal transit especially during stomach and intestinal residence are also analyzed. In order to understand the adaptation mechanisms of probiotic bacteria to gastrointestinal stress, intrinsic and adaptive mechanisms identified in probiotic strains in response to acid stress and to bile and bile acid stress are analyzed. In addition, improvement strategies for multiple stress tolerance of lactic acid bacteria through directions dealing with stress, accumulation of metabolites, use of protectants, and regulation of technological parameters are examined. Finally, the definition of postbiotics, inanimate microorganisms and/or their components conferring health benefits, is also introduced. Postbiotics include cell lysates, enzymes, and cell wall fragments derived from probiotic bacteria and may represent an alternative to the use of probiotics, when they do not tolerate stressful conditions.

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          Antioxidants Maintain Cellular Redox Homeostasis by Elimination of Reactive Oxygen Species.

          Reactive oxygen species (ROS) are produced by living cells as normal cellular metabolic byproduct. Under excessive stress conditions, cells will produce numerous ROS, and the living organisms eventually evolve series of response mechanisms to adapt to the ROS exposure as well as utilize it as the signaling molecules. ROS molecules would trigger oxidative stress in a feedback mechanism involving many biological processes, such as apoptosis, necrosis and autophagy. Growing evidences have suggested that ROS play a critical role as the signaling molecules throughout the entire cell death pathway. Overwhelming production of ROS can destroy organelles structure and bio-molecules, which lead to inflammatory response that is a known underpinning mechanism for the development of diabetes and cancer. Cytochrome P450 enzymes (CYP) are regarded as the markers of oxidative stress, can transform toxic metabolites into ROS, such as superoxide anion, hydrogen peroxide and hydroxyl radical which might cause injury of cells. Accordingly, cells have evolved a balanced system to neutralize the extra ROS, namely antioxidant systems that consist of enzymatic antioxidants such as superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidases (GPxs), thioredoxin (Trx) as well as the non-enzymatic antioxidants which collectively reduce oxidative state. Herein, we review the recent novel findings of cellular processes induced by ROS, and summarize the roles of cellular endogenous antioxidant systems as well as natural anti-oxidative compounds in several human diseases caused by ROS in order to illustrate the vital role of antioxidants in prevention against oxidative stress.
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            Bifidobacteria and Their Role as Members of the Human Gut Microbiota

            Members of the genus Bifidobacterium are among the first microbes to colonize the human gastrointestinal tract and are believed to exert positive health benefits on their host. Due to their purported health-promoting properties, bifidobacteria have been incorporated into many functional foods as active ingredients. Bifidobacteria naturally occur in a range of ecological niches that are either directly or indirectly connected to the animal gastrointestinal tract, such as the human oral cavity, the insect gut and sewage. To be able to survive in these particular ecological niches, bifidobacteria must possess specific adaptations to be competitive. Determination of genome sequences has revealed genetic attributes that may explain bifidobacterial ecological fitness, such as metabolic abilities, evasion of the host adaptive immune system and colonization of the host through specific appendages. However, genetic modification is crucial toward fully elucidating the mechanisms by which bifidobacteria exert their adaptive abilities and beneficial properties. In this review we provide an up to date summary of the general features of bifidobacteria, whilst paying particular attention to the metabolic abilities of this species. We also describe methods that have allowed successful genetic manipulation of bifidobacteria.
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              Gut Microbiome: Profound Implications for Diet and Disease

              The gut microbiome plays an important role in human health and influences the development of chronic diseases ranging from metabolic disease to gastrointestinal disorders and colorectal cancer. Of increasing prevalence in Western societies, these conditions carry a high burden of care. Dietary patterns and environmental factors have a profound effect on shaping gut microbiota in real time. Diverse populations of intestinal bacteria mediate their beneficial effects through the fermentation of dietary fiber to produce short-chain fatty acids, endogenous signals with important roles in lipid homeostasis and reducing inflammation. Recent progress shows that an individual’s starting microbial profile is a key determinant in predicting their response to intervention with live probiotics. The gut microbiota is complex and challenging to characterize. Enterotypes have been proposed using metrics such as alpha species diversity, the ratio of Firmicutes to Bacteroidetes phyla, and the relative abundance of beneficial genera (e.g., Bifidobacterium, Akkermansia) versus facultative anaerobes (E. coli), pro-inflammatory Ruminococcus, or nonbacterial microbes. Microbiota composition and relative populations of bacterial species are linked to physiologic health along different axes. We review the role of diet quality, carbohydrate intake, fermentable FODMAPs, and prebiotic fiber in maintaining healthy gut flora. The implications are discussed for various conditions including obesity, diabetes, irritable bowel syndrome, inflammatory bowel disease, depression, and cardiovascular disease.
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                Author and article information

                Contributors
                t.varzakas@uop.gr
                Journal
                Probiotics Antimicrob Proteins
                Probiotics Antimicrob Proteins
                Probiotics and Antimicrobial Proteins
                Springer US (New York )
                1867-1306
                1867-1314
                3 June 2024
                3 June 2024
                2025
                : 17
                : 1
                : 138-158
                Affiliations
                [1 ]Centro de Investigación en Biofísica Aplicada y Alimentos (CIBAAL/UNSE-CONICET), RN 9-Km 1125, (4206), Santiago del Estero, Argentina
                [2 ]Facultad de Agronomía y Agroindustrias (FAyA), Universidad Nacional de Santiago del Estero, ( https://ror.org/01v9p7c03) Av. Belgrano Sur 1912, (4200), Santiago del Estero, Argentina
                [3 ]Facultad de Humanidades, Ciencias Sociales y de La Salud (FHU), Universidad Nacional de Santiago del Estero, ( https://ror.org/01v9p7c03) Av. Belgrano Sur 1912, (4200), Santiago del Estero, Argentina
                [4 ]Centro de Referencia Para Lactobacilos (CONICET-CERELA), ( https://ror.org/03cqe8w59) Chacabuco 145, (4000), San Miguel de Tucumán, Argentina
                [5 ]Department of Food Science and Technology, University of the Peloponnese, ( https://ror.org/04d4d3c02) 24100 Antikalamos Messinia, Kalamata, Greece
                [6 ]Laboratory of Microbial Biotechnology and Engineering Enzymes (LMBEE), Center of Biotechnology of Sfax (CBS), University of Sfax, ( https://ror.org/04d4sd432) Road of Sidi Mansour Km 6, P.O. Box 1177, 3018 Sfax, Tunisia
                [7 ]Institute of Bioproduct Development (IBD), Universiti Teknologi Malaysia (UTM), ( https://ror.org/026w31v75) 81310 Johor, Malaysia
                [8 ]Faculty of Chemical and Energy Engineering, Universiti Teknologi Malaysia (UTM), ( https://ror.org/026w31v75) 81310 Johor, Malaysia
                [9 ]City of Scientific Research and Technology Applications (SRTA), ( https://ror.org/00pft3n23) New Borg Al Arab, 21934 Egypt
                Article
                10273
                10.1007/s12602-024-10273-9
                11832585
                38829565
                e8d55c90-c2b9-430c-a00c-b3397d0da37e
                © The Author(s) 2024

                Open Access 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://creativecommons.org/licenses/by/4.0/.

                History
                : 20 April 2024
                Funding
                Funded by: University of Peloponnese
                Categories
                Review
                Custom metadata
                © Springer Science+Business Media, LLC, part of Springer Nature 2025

                Microbiology & Virology
                probiotics,functional foods,stress conditions,gastrointestinal passage,postbiotics

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