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An Investigation of the Prebiotic Properties of Australian Honeys

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An Investigation of the Prebiotic Properties of Australian Honeys An investigation of the prebiotic properties of Australian honeys Nural Cokcetin A thesis in fulfilment of the requirements for the degree of Doctor of Philosophy School of Biotechnology and Biomolecular Sciences Faculty of Science April 2015 THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet Surname or Family name: Cokcetin First name: Nural Other name/s: Abbreviation for degree as given in the University calendar: PhD School: School of Biotechnology and Biomolecular Sciences Faculty: Science Title: An investigation of the prebiotic properties of Australian honeys ABSTRACT Non-digestible carbohydrates that promote specific, favourable changes in the composition and functionality of the gut microbiota, and thus contribute to improving health and well-being, are referred to as prebiotics. These favourable changes might be due to a relative increase in the numbers of potentially beneficial bacteria, and/or an increase in the metabolic activity of gut microbiota to produce more beneficial substances, such as short chain fatty acids (SCFA). An established method for quantifying the prebiotic effect of a carbohydrate utilises the Prebiotic Index (PI), which is the ratio of the changes in the populations of the potentially beneficial and potentially harmful bacteria. Honey contains non-digestible oligosaccharides and there is some evidence that certain honeys could induce beneficial changes in the gut, however there is limited information on Australian floral varieties of honey. The aim of this work was to conduct an in-depth investigation of the prebiotic properties of Australian honeys from a variety of floral sources. Three broad approaches were used. Initially, the influences of the monosaccharides in high fructose content Australian honeys on the composition and metabolic activity of gut microbes were tested in microcosms established with human intestinal microbiota. Secondly, the impact of the monosaccharides and non-digestible components (oligosaccharides) found naturally in honey on the growth and metabolic function of the gut microbiota was tested. The non-digestible components were obtained by simulating gastrointestinal conditions using a digestion process that mimicked the upper regions of the gastrointestinal tract. Both whole and digested honeys were assayed in microcosms established using human intestinal microbiota to simulate the lower regions of the gastrointestinal tract. Standard culture-based techniques were used to determine the impact of the honey monosaccharides and oligosaccharides on the numbers of the major bacterial groups of the gut. Molecular profiling of the microcosm microbiota enriched with four of the honeys supported the data from the culture-based methodology. The PI values of the honeys were determined, and the effect of the honeys on SCFA production by the gut microbiota was measured. Finally, the effect of the in vitro fermentation of honey by the gut microbiota on the growth of three enteropathogens and a probiotic strain was determined as an assessment of the resilience of the microcosm to an introduced species. It was shown that the saccharides present in honey affected the bacterial composition of the gut microbiota. While much of the compositional changes can be attributed to the complex sugars that remain after digestion (oligosaccharides), the simple sugars (monosaccharides) in honey also contributed to modulation of the gut microbiota. The presence of the monosaccharides in honey significantly affected the changes in the microbial composition. Positive changes in the potentially beneficial lactobacilli populations were observed when high fructose content honeys were used, and these effects were attributed to the fructose components of the honeys. The second part of this study focused on the oligosaccharide components of the honey. This was the first study to investigate the impact of simulated digestion of Australian honeys on their prebiotic activity. The oligosaccharide components of all of the tested varieties of Australian honeys exerted favourable effects on the gut ecosystem by promoting the growth of the beneficial bacteria at levels similar to commercial prebiotic, inulin. The honeys suppressed the potentially harmful populations of the gut, and the growth of clostridia specifically was significantly impaired in the presence of the honeys. All honeys had positive PI values, and they also enhanced the production of SCFA, especially the butyric acid, but both of these parameters varied considerably depending on the honey type. Finally, the fermentation of honey by human gut microbiota resulted in the production of compounds with inhibitory activity against three common enteropathogens, namely Salmonella typhimurium, Clostridium difficile and Escherichia coli, and at levels that matched the commercial prebiotic control, inulin. Most of the honeys tested were more effective at inhibiting the growth of C. difficile than the prebiotic control, and inclusion of inulin in the microcosms had little added inhibitory effect on C. difficile growth, suggesting that the honeys allowed enhanced production of the inhibitory substances. These compounds did not inhibit the growth of a commercial beneficial probiotic strain, Lactobacillus fermentum. In summary, the results from this investigation demonstrate that Australian honeys have considerable prebiotic capacity which was comparable to or better than inulin. The prebiotic properties of the honeys were associated with the fructose and the oligosaccharides of the honeys which promoted the beneficial bacteria, inhibited the potential pathogens and elevated butyric acid levels. Declaration relating to disposition of project thesis/dissertation I hereby grant to the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or in part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all property rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstracts International (this is applicable to doctoral theses only). …………………………………………………………… ……………………………………..……………… ……….…………………….. Signature Witness .…….… Date The University recognises that there may be exceptional circumstances requiring restrictions on copying or conditions on use. Requests for restriction for a period of up to 2 years must be made in writing. Requests for a longer period of restriction may be considered in exceptional circumstances and require the approval of the Dean of Graduate Research. FOR OFFICE USE ONLY Date of completion of requirements for Award: Originality statement ‘I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or in style, presentation and linguistic expression is acknowledged.’ Signed …………………………………………….............. Date …………………………………………….............. i Abstract Non-digestible carbohydrates that promote specific, favourable changes in the composition and functionality of the gut microbiota, and thus contribute to improving health and well-being, are referred to as prebiotics. These favourable changes might be due to a relative increase in the numbers of potentially beneficial bacteria, and/or an increase in the metabolic activity of gut microbiota to produce more beneficial substances, such as short chain fatty acids (SCFA). An established method for quantifying the prebiotic effect of a carbohydrate utilises the Prebiotic Index (PI), which is the ratio of the changes in the populations of the potentially beneficial and potentially harmful bacteria. Honey contains non-digestible oligosaccharides and there is some evidence that certain honeys could induce beneficial changes in the gut, however there is limited information on Australian floral varieties of honey. The aim of this work was to conduct an in-depth investigation of the prebiotic properties of Australian honeys from a variety of floral sources. Three broad approaches were used. Initially, the influences of the monosaccharides in high fructose content Australian honeys on the composition and metabolic activity of gut microbes were tested in microcosms established with human intestinal microbiota. Secondly, the impact of the monosaccharides and non-digestible components (oligosaccharides) found naturally in honey on the growth and metabolic function of the gut microbiota was tested. The non-digestible components were obtained by simulating gastrointestinal conditions using a digestion process that mimicked the upper regions of the gastrointestinal tract. Both whole and digested honeys were assayed in microcosms established using human intestinal microbiota to simulate the lower regions of the gastrointestinal tract. Standard
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