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Departamento De Biotecnología Identificación De Componentes De Departamento de Biotecnología Identificación de componentes de la microbiota intestinal potencialmente beneficiosos frente a la obesidad MEMORIA DE TESIS PRESENTADA POR Eva Mª Gómez del Pulgar Villanueva PARA OPTAR AL GRADO DE DOCTOR EN BIOTECNOLOGÍA POR LA UNIVERSIDAD POLITÉCNICA DE VALENCIA DIRECTORES: Dra. Yolanda Sanz Herranz Dr. Alfonso Benítez-Páez Valencia, noviembre de 2018 2 La Dra Yolanda Sanz Herranz, Profesora de Investigación del CSIC, perteneciente al Instituto de Agroquímica y Tecnología de Alimentos (IATA) de Valencia. CERTIFICA: que la Licenciada en Biotecnología Eva Mª Gómez del Pulgar Villanueva ha realizado bajo su dirección en el Instituto de Agroquímica y Tecnología de Alimentos el trabajo que lleva por título “Identificación de componentes de la microbiota intestinal potencialmente beneficiosos frente a la obesidad”, y autoriza su presentación para optar al grado de Doctor. Y para que así conste, expido y firmo el presente certificado en Valencia, a 16 de octubre de 2018. Dra. Yolanda Sanz Herranz 3 4 A mi familia, A ti. 5 6 RESUMEN La obesidad es un problema de salud a nivel mundial que incrementa el riesgo de sufrir un amplio rango de comorbilidades, incluyendo la diabetes tipo II y las enfermedades cardiovasculares. Estas patologías pueden estar precedidas por el síndrome metabólico, definido como una agrupación de marcadores de riesgo cardiometabólico, incluyendo la obesidad abdominal, el desequilibrio en la homeostasis de la glucosa, la dislipidemia y la hipertensión. La obesidad y el sobrepeso causan cada vez más muertes cada año y se estima que aproximadamente un cuarto de la población adulta sufre síndrome metabólico. Debido a estos motivos, es necesario encontrar estrategias para reducir la obesidad y sus co-morbilidades y que puedan ser implementadas en los sistemas de salud públicos. El objetivo general de la tesis ha sido avanzar en el conocimiento de la influencia de la composición y funciones de la microbiota intestinal y su genoma (microbioma) en la obesidad y alteraciones metabólicas asociadas e identificar bacterias intestinales que, junto a cambios en la dieta, puedan contribuir a establecer estrategias de intervención más eficaces para controlar estos desórdenes. El capítulo primero de la tesis se centra en el estudio de la seguridad y habilidad para metabolizar distintas fuentes de fibra de Bacteroides uniformis CECT 7771, una cepa que demostró capacidad para reducir las alteraciones metabólicas asociadas a la obesidad inducida por la dieta en estudios pre- clínicos previos. Para ello, hemos llevado a cabo la secuenciación del genoma y el análisis del transcriptoma de la bacteria en respuesta a diferentes fuentes de carbono (glucosa, salvado de trigo, pectina, mucina, goma arábiga e inulina). Se ha observado que B. uniformis CECT7771 es capaz de fermentar todos los sustratos evaluados y crecer más rápido en presencia de aquellas fuentes de carbono de estructura más sencilla (salvado de trigo rico en arabinoxilanos (AXOS) y glucosa). Además, B.uniformis CECT 7771 posee la capacidad de degradar los O-glicanos de la mucina y producir butirato y disminuir la producción de ácidos grasos de cadena larga y proteínas transportadoras de acilo (ACPs), implicados en la síntesis de lipopolisacárido (LPS) bacteriano causante de endotoxemia. Cuando crece en presencia de pectina, B. uniformis CECT 7771 incrementa la producción y secreción de GABA, lo cual podría tener un impacto en el eje intestino-cerebro. B. uniformis CECT 7771 no ha mostrado signos de toxicidad o patogenicidad tras el análisis exhaustivo de los genes codificados en su genoma, ni tras su administración por vía oral en un modelo de toxicidad sub-crónica en ratas. 7 En este modelo, la bacteria produce un perfil de citocinas anti-inflamatorio comparado con el grupo placebo y muestra un efecto dosis-dependiente en la disminución de los valores de la alanina aminotransferasa (ALT), sugiriendo un efecto hepato-protector. En el segundo capítulo de la tesis se ha llevado a cabo un estudio de intervención en humanos con sobrepeso y síndrome metabólico en el que se evaluó, en un primer lugar, los efectos de la suplementación dietética con fibras enriquecidas en AXOS y ácidos grasos poliinsaturados (PUFAs) durante 4 semanas en la composición de la microbiota intestinal y en los parámetros bioquímicos (medidas antropométricas, metabolismo de glucosa, perfil lipídico, marcadores de inflamación, etc.). Los resultados demuestran que la ingesta de AXOS modifica la microbiota, ejerciendo un efecto bifidogénico y un aumento de especies bacterianas productoras de butirato, aunque no hemos visto una mejora en los parámetros bioquímicos analizados. En el caso de la intervención con PUFAs, no hemos detectado cambios en la composición de la microbiota ni en los parámetros bioquímicos evaluados. En segundo lugar, hemos llevado a cabo un estudio multi-ómico en un subgrupo de sujetos de la intervención con AXOS a fin de profundizar en los efectos de este tipo de fibra. El análisis metagenómico nos ha permitido identificar cambios en la configuración de la microbiota intestinal, incluyendo un aumento de Ruminococcus gnavus y Prevotella spp. así como una disminución de Parabacteroides, Paraprevotella y Rikenella. También hemos detectado un incremento de metagenes implicados en la producción de tetrahidrofolato y derivados del ácido fólico, los cuales llevan a cabo una función protectora frente a la hiperhomocisteinemia; la vitamina K2, implicada en la correcta absorción del calcio; y el GABA, cuya baja concentración en el organismo se asocia a estados de ansiedad y desbalance energético y que favorece la secreción de insulina y regula los niveles de ceramidas en plasma. El análisis conjunto del metagenoma y el metaboloma nos ha permitido establecer correlaciones positivas entre la abundancia de Prevotella y las concentraciones de ácidos grasos de cadena corta y succinato, así como entre aumentos de Eubacterium rectale y reducciones en metilaminas, que podrían estar implicadas en la mejora del metabolismo de glucosa y reducción del riesgo de sufrir patologías crónicas. Además, el análisis lipidómico demuestra una reducción de las ceramidas en plasma, que sugieren mejoría del metabolismo de la glucosa. La integración de datos multi-omicos sugieren, globalmente, que la ingesta de AXOS podría contribuir especialmente al mantenimiento de la homeostasis de la glucosa en individuos con sobrepeso. 8 RESUM L'obesitat és un problema de salut a nivell mundial que incrementa el risc de patir un ampli rang de comorbilitats, incloent la diabetis tipus II i les malalties cardiovasculars. Estes patologies poden estar precedides per la síndrome metabòlica, definit com una agrupació de marcadors de risc cardiometabólic, incloent l'obesitat abdominal, el desequilibri en l'homeostasis de la glucosa, la dislipidemia i la hipertensió. L'obesitat i la sobrecàrrega causen cada vegada més morts cada any i s'estima que aproximadament un quart de la població adulta patix síndrome metabòlica. A causa d'estos motius, és necessari trobar estratègies per a reduir l'obesitat i les seues comorbilitats i que puguen ser implementades en els sistemes de salut públics. L'objectiu general de la tesi ha sigut avançar en el coneixement de la influència de la composició i funcions de la microbiota intestinal i el seu genoma (microbioma) en l'obesitat i alteracions metabóliques associades i identificar bacteris intestinals que, junt amb canvis en la dieta, puguen contribuir a establir estratègies d'intervenció més eficaços per a controlar estos desordes. El capítol primer de la tesi es centra en l'estudi de la seguretat i habilitat per a metabolitzar distintes fonts de fibra de Bacteroides uniformis CECT 7771, una cepa que va demostrar capacitat per a reduir les alteracions metabòliques associades a l'obesitat induïda per la dieta en estudis preclínics previs. Per a això, hem dut a terme la seqüenciació del genoma i l'anàlisi del transcriptoma del bacteri en resposta a diferents fonts de carboni (glucosa, segó de blat, pectina, mucina, goma aràbiga i inulina). S'ha observat que B. uniformis CECT7771 és capaç de fermentar tots els substrats avaluats i créixer més ràpid en presència d'aquelles fonts de carboni d'estructura més senzilla (segó de blat ric en arabinoxilans (AXOS) i glucosa). A més, B.uniformis CECT 7771 posseïx la capacitat de degradar els O- glicans de la mucina i produir butirat i disminuir la producció d'àcids grassos de cadena llarga i proteïnes transportadores d'acil (ACPs), implicades en la síntesi de lipopolisacárid (LPS) bacterià causant d'endotoxemia. Quan creix en presència de pectina, B. uniformis CECT 7771 incrementa la producció i secreció de GABA, la qual cosa podria tindre un impacte en l'eix intestí- cervell. B. uniformis CECT 7771 no ha mostrat signes de toxicitat o patogenicidad després de l'anàlisi exhaustiva dels gens codificats en el seu genoma, ni després de la seua administració per via oral en un model de toxicitat subcrònica en rates. En este model, el bacteri produïx un perfil de citoquines antiinflamatori comparat amb el grup placebo i mostra un efecte 9 dosi- dependent en la disminució dels valors de l'alanino aminotransferasa (ALT), suggerint un efecte hepato-protector. En el segon capítol de la tesi s'ha dut a terme un estudi d'intervenció en humans amb sobrecàrrega i síndrome metabòlica en què es va avaluar, en un primer lloc, els efectes de la suplementació dietètica amb fibres enriquides en AXOS i àcids grassos poliinsaturats (PUFAs) durant 4 setmanes en la composició de la microbiota intestinal i en els paràmetres bioquímics (mesures antropomètriques, metabolisme de glucosa, perfil lipídic, marcadors d'inflamació, etc.). Els resultats demostren que la ingesta d'AXOS modifica la microbiota, exercint un efecte bifidogénic i un augment d'espècies bacterianes productores de butirat, encara que no hem vist una millora en els paràmetres bioquímics analitzats. En el cas de la intervenció amb PUFAs, no hem detectat canvis en la composició de la microbiota ni en els paràmetres bioquímics avaluats. En segon lloc, hem dut a terme un estudi multi-ómic en un subgrup de subjectes de la intervenció amb AXOS a fi d'aprofundir en els efectes d'este tipus de fibra.
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