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Universidade De Lisboa Faculdade De Medicina Veterinária UNIVERSIDADE DE LISBOA FACULDADE DE MEDICINA VETERINÁRIA MODULATION OF RUMINAL BIOHYDROGENATION IN SHEEP THROUGH DIETARY TANNINS OR ENERGY SOURCES MÓNICA MENDES DA COSTA Orientador: Professor Doutor Rui José Branquinho de Bessa Tese especialmente elaborada para obtenção do grau de Doutor em Ciências Veterinárias na Especialidade de Produção Animal 2017 UNIVERSIDADE DE LISBOA FACULDADE DE MEDICINA VETERINÁRIA MODULATION OF RUMINAL BIOHYDROGENATION IN SHEEP THROUGH DIETARY TANNINS OR ENERGY SOURCES MÓNICA MENDES DA COSTA Orientador: Professor Doutor Rui José Branquinho De Bessa Tese especialmente elaborada para obtenção do grau de Doutor em Ciências Veterinárias na Especialidade de Produção Animal Júri: Presidente: Doutor Rui Manuel Vasconcelos e Horta Caldeira Vogais: - Doutor Carlos Mendes Godinho de Andrade Fontes - Doutor Miguel António Machado Rodrigues - Doutor Rui José Branquinho de Bessa - Doutor José Manuel Bento Santos Silva - Doutora Margarida Rosa Garcez Maia 2017 I dedicate this thesis to My parents and my sister My grandparents Acknowledgements I want to thank to the following entities and people because without them the work presented in this thesis would not be accomplished: To Foundation for Science and Technology (FCT) for my PhD fellowship and the project that financed the work. To the Faculty of Veterinary Medicine, University of Lisbon (FMV-UL), for being the place were I spent twelve years studying and working, not only for my PhD but also for previous research and integrated master in Veterinary Medicine. To Centre for Interdisciplinary Research in Animal Health (CIISA), for all the facilities and materials necessary for my PhD work. To Professor Rui José Branquinho de Bessa, for being my supervisor during my PhD while providing me with some of his vast knowledge, mainly in experimental design and statistics, and for all his suggestions and corrections during my journey through the Animal Production research field that were indispensable for the elaboration of the thesis and research articles. I want also to thank him for the financial support for all the work developed and for allowing me the opportunity of going abroad for research and work presentation. To Doctor Susana Paula Alves, for all the help during my PhD work, mainly with fatty acid analysis and development of the corresponding analytical methodologies, as well as with the management of the animals and samples collection and assistance with the elaboration of the thesis and research articles. To Doctor José Manuel Bento Santos Silva, for being indispensable in the experiment implemented in National Institute of Agrarian and Veterinarian Research (INIAV) (Santarém), especially in the animal management, interpretation of results and elaboration of the research article, and for the great hospitality during my stay in INIAV facilities. To Professor José Prates, Doctor Cristina Alfaia and Doctor Susana Martins, for the contributions on conjugated fatty acid and gene analyses performed in the last experiment. i To Professor Tim McAllister, for giving me the opportunity to stay in his home during my work in Canada and for the knowledge transmitted and his friendship. To Master Krysty Munns, for receiving me so well in Canada, and to Doctor Shaun Cook, for all the help with the laboratory work developed in Canada and for the knowledge about the analytical methodologies for quantification of rumen bacteria. To Professor Ana Duarte, for all the knowledge transmitted that was essential for the quantification of rumen bacteria. To Doctor Annabelle Troegeler-Meynadier and to Professor Francis Enjalbert, for the analysis of samples from rumen content using pyrosequencing, providing me with the corresponding data. To Enginneer Suzette Mota, for the help in animal management; to Paula Santos, for lambs slaughtering and processing of carcasses; and to Doctor João Almeida, for the help in meat quality analysis. To Ângelo Cabo, Olinda Guerreiro and Alice Cappucci, for the help with some of the experiments. To Professor Victor Diogo Alves, for the friendship and assistance with the elaboration of the thesis. To Margarida Aguiar, for the support in the end of my PhD work. To Tiago Calado, a family friend, for his informatic assistance. To Bruno Costa, for the friendship, pacience and support when I was writing the thesis. To my parents, sister and grandparents, for being the foundations of my work, contributing for the person that I am now and, consequently, without them none of my PhD work would be possible. ii This work was financed by Fundação para a Ciência e Tecnologia (FCT) through the individual fellowship SFRH/BD/90468/2012 and co-financed by the grants PTDC/CVT/120122/2010 and UID/CVT/00276/2013 iii Abstract Modulation of ruminal biohydrogenation in sheep through dietary tannins or energy sources In the present thesis, four experiments were conducted to study how ruminal biohydrogenation pathways can be modulated through dietary inclusion of tannin sources and to acquire a better comprehension about the occurence of t10-shifted biohydrogenation pathways. In the first experiment, in vitro batch incubations with 100 g/kg dry matter (DM) of extracts of chestnut tannins (mostly hydrolysable tannins) and quebracho, grape seed or rockrose (Cistus ladanifer) condensed tannins, as well as a control treatment were incubated for 6 h with ruminal fluid from fistulated sheep and a dehydrated lucerne-based substrate with 60 g/kg DM of sunflower oil. Grape seed and, to a lesser extent, C. ladanifer led to a higher disappearance of 18:2n-6 with a consequent higher production of c9,t11-18:2 and t11- 18:1 than chestnut, quebracho and control. There was no clear innibition of 18:0 production with any of the extracts comparing with control. In the second experiment, rumen fistulated sheep were fed tannin extracts from mimosa condensed tannins, chestnut hydrolysable tannins or their mixture (100 g/kg DM) in a complete diet with sunflower and linseed oils (40 g/kg DM), following a change-over design (3 treatments, 4 sheep and 4 periods). There was a variable inhibition of ruminal biohydrogenation and a lower “trans-/cis-18:1” ratio in bacterial fractions with mimosa than with chestnut. Mimosa led to a lower fermentative activity, as well as a lower abundance of Fibrobacter succinogenes, Ruminococcus albus, Ruminococcus flavefaciens and Butyrivibrio proteoclasticus and higher abundance of Selenomonas ruminantium with a lower bacterial biomass estimate of dimethylacetals than chestnut. In the third experiment, two rumen fistulated rams were housed in metabolic cages and adapted to a wheat-based diet with 41 g/kg DM of sunflower oil. During the first two weeks of trial, the t10-shift occurred temporarily in both animals but in different moments. These results were probably due to individual variability of rumen microbiota, since, for a selected period of the trial, a lower bacterial diversity was found for ram 1 compared to ram 2. Moreover, the t10-shift was associated with an increase of total trans-18:1 and a decrease of 18:0. There was no clear association of t10-shift with rumen pH or its expression in blood plasma. In the fourth experiment, 40 lambs were fed, for 6 weeks, with complete diets containing barley or barley completely replaced for dehydrated citrus pulp, dehydrated beet pulp or soybean hulls. All diets were supplemented with an oil blend (soybean:fish oils, 59:10 g/kg DM). Overall, the t10-/t11-18:1 ratio was above 3 in meat and subcutaneous fat, although soybean hulls increased t11-18:1 and c9,t11-18:2 comparing with the other treatments. Citrus pulp led to the lowest gene expression of fatty acid synthase, while that of stearoyl-CoA desaturase was inferior for soybean hulls and beet pulp. Keywords: Fatty acids, biohydrogenation, rumen bacteria, tannins, starch. iv Resumo Modulação da bioidrogenação ruminal em ovinos através de taninos ou de fontes energéticas da dieta A dieta dos ruminantes é um dos principais determinantes que influencia a bioidrogenação (BH) ruminal. A inclusão de taninos na dieta, os quais são compostos fenólicos das plantas, pode aumentar a proporção, no rúmen e nos tecidos, de ácidos gordos (AG) bioactivos com efeitos benéficos na saúde humana, tais como os ácidos vacénico (t11-18:1) e ruménico (c9,t11-18:2; conjugado do ácido linoleico - CLA) derivados das vias t11 da BH. A maior quantidade de c9,t11-18:2 presente nos tecidos resulta da dessaturação de t11-18:1 pela estearoil-CoA dessaturase (SCD; Δ9-dessaturase). Contudo, na presença de dietas com alto teor em amido e baixo conteúdo em forragem, com ou sem suplementação com óleos ricos em ácidos gordos polinsaturados, pode ocorrer uma modificação das vias da BH com predomínio das vias t10 relativamente às t11 (o shift-t10) e o concomitante aumento de AG deletérios para a saúde, nomeadamente t10-18:1 e t10,c12-18:2. Na presente tese, foram realizadas duas experiências com o propósito de estudar o efeito da inclusão de diversos tipos de taninos como moduladores da BH (experiências 1 e 2) e duas experiências para obter uma melhor compreensão dos factores que determinam a ocorrência do shift-t10 (experiências 3 e 4). Em todos os estudos, foram incorporados óleos de origem vegetal ou animal nas dietas para aumentar a formação de intermediários da BH. Na primeira experiência, foi realizado um ensaio in vitro com 100 g/kg de matéria seca (MS) de extractos de taninos da castanha (maioritariamente taninos hidrolisáveis) e de extractos de taninos condensados de quebracho, de sementes de uva e de esteva (Cistus ladanifer), bem como um tratamento controlo (sem taninos). As incubações decorreram durante 6 h com fluido de rúmen de ovinos fistulados e um substrato à base de luzerna desidratada com 60 g/kg MS de óleo de girassol (2:1, rácio “foragem/concentrado”). A composição em AG dos tubos de incubação foi obtida por transesterificação combinada, seguida da separação dos ésteres metílicos dos AG por cromatografia gás-líquido e da sua identificação com espectrometria de massa.
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