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Centro De Investigación Y De Estudios Avanzados Del CENTRO DE INVESTIGACIÓN Y DE ESTUDIOS AVANZADOS DEL INSTITUTO POLITÉCNICO NACIONAL UNIDAD IRAPUATO DEPARTAMENTO DE INGENIERÍA GENÉTICA AISLADOS DE COMUNIDADES DE SEDIMENTO DE CUATROCIÉNEGAS, COAHUILA COMO MODELO PARA ANALIZAR LA COHERENCIA FENOTÍPICA DEL GÉNERO BACILLUS Tesis que presenta M.C. MARIA DOLORES RODRIGUEZ TORRES Para Obtener el Grado de Doctora en Ciencias En la Especialidad de Biotecnología de Plantas Directora de la Tesis: Dra. Gabriela Olmedo Álvarez AGRADECIMIENTOS Agradezco el apoyo financiero otorgado por el CONACYT con la beca número 229493 para la realización de este trabajo de investigación. Al CINVESTAV por la oportunidad que me dieron para realizar mis estudios dentro de la institución y permitirme forjar la pasión por la investigación. A la Dra. Gabriela Olmedo Álvarez por su gran paciencia, su apoyo y permitirme trabajar en el laboratorio de Biología Molecular y Ecología Microbiana. A la Dra. Valeria Souza Saldívar por compartir su pasión por nuestro lugar de estudio: Cuatrociénegas, Coahuila. A los Doctores: Laila Pamela Partida Martínez, Jorge Eugenio Ibarra Rendón, Alexander de Luna Fors, Rafael Rivera Bustamante, por sus valiosas sugerencias y aportaciones a lo largo de estos años. A los miembros del Laboratorio de Metabolómica y Fisiología Molecular y al Laboratorio Biología de Sistemas Genéticos, por permitirme utilizar sus equipos. A la M.C. Africa Islas Robles por su dedicación en el trabajo, el apoyo brindado y la amistad. Al grupo de seminarios de microorganismos. A todos los colaboradores y amigos que participaron en la elaboración y diseño de experimentos, análisis y discusiones: Zulema Gómez Lunar, Ismael Hernández González, Varinia López, Julio Cruz Medina, José Antonio González, Adrian Jinich, Yunuen Tapia, Luis J. Delaye, Paul Decena, Susana de la Torre, Mayra E. Covaxin, José Antonio Cisneros, J. Eugenio Reynoso. A mis papás, por su gran apoyo y enseñanzas. A mis hermanos, Ricardo, Pablo y Liliana. A mis sobrinos, Montse, Pau, Erik y Vale, que son la alegría de la casa. A mi esposo Abul, por la paciencia, tolerancia y amor. ÍNDICE Agradecimientos i Índice ii Índice de tablas iii Índice de figuras iv Resumen 1 Abstract 2 1. INTRODUCCIÓN 3 2. ANTECEDENTES 7 2.1 Comunidades microbianas y distribución 7 2.1.1 Procesos de ensamble de la comunidad: Filtrado del hábitat y 8 competencia 2.2 Demarcación de especies bacterianas y coherencia ecológica 10 2.2.1 Definición de especies 10 2.2.2 Coherencia ecológica de especies 11 2.3 Comportamiento social de los microorganismos dentro de las 13 comunidades y los rasgos fenotípicos 2.4 El género Bacillus 16 2.4.1 Generalidades del género Bacillus 16 2.3.2 Hábitat del género Bacillus 18 2.3.4 Comportamiento social y multicelularidad del género Bacillus 18 2.4 Cuatro Ciénegas Coahuila 20 3. HIPÓTESIS 22 4. OBJETIVOS 23 4.1 Objetivo general 23 4.2 Objetivos específicos 23 5 MATERIALES Y MÉTODOS 24 5.1 Sitio de estudio 24 5.2 Muestreo y aislamiento bacteriano 24 5.3 Extracción de DNA, marcadores moleculares y construcción 25 filogenética 5.4 Análisis filogenético de las comunidades de aislados 26 termoresistentes 5.5 Ensayos fenotípicos de una sub-muestra de 141 Bacillus spp. 27 5.6 Evaluación de la capacidad de las cepas de Bacillus spp. para 29 crecer en diferentes fuentes de fósforo 5.7 Señal filogenética de los rasgos de Bacillus spp. 30 5.8 Preparación de muestras para microscopía electrónica de 30 transmisión 5.9 Clasificación de cepas de Bacillus spp. para identificación de 31 proteínas ribosomales usando espectrometría de masas 5.10 Análisis estadístico 32 6. RESULTADOS 33 6.1 Todos los grupos taxonómicos de los aislados termoresistentes no 33 están aleatoriamente dispersos entre los sitios de muestreo. 6.2 Coherencia por las preferencias por la utilización de fuentes de 35 carbono entre los linajes de Bacillus spp 6.3 Variación extensiva de rasgos profundamente enraizados 39 relacionados en rasgos de acción colectiva 6.4 Una paradoja de extensas auxotrofías entre algunos clados de 42 Bacillus spp. 6.5 Distribución de rasgos profundamente enraizados de los Bacillus 43 spp. en comunidades de sedimento exhiben poca señal filogenética y en su lugar es consistente con un modelo Browniano 6.6 Morfología de la colonia y pigmentación son rasgos altamente 46 conservados, rasgos de clado específico 6.7 Sobredispersión en las preferencias por la utilización de fuentes de 48 fósforo entre los linajes de Bacillus 6.8 Imágenes obtenidas con el microscopio electrónico de transmisión 49 de cepas de Bacillus spp 6.9 Clasificación de Bacillus por Maldi-Tof y análisis filogenético con los 52 genes 16S rRNA y gltX 7. DISCUSIÓN 59 7.1 ¿Qué tanta variabilidad filogenética hay entre los aislados 61 individuales a nivel superficial y profundo? 7.2 ¿La evolución trabaja a nivel individual o a nivel de la comunidad? 65 7.3 ¿Podrían algunos clados, como el de B. cereus, basar su éxito en 66 compartir funciones a nivel comunidad? 8. CONCLUSIONES 67 9. PERSPECTIVAS 68 10. REFERENCIAS BIBLIOGRÁFICAS 70 ÍNDICE DE TABLAS Tabla 1. Tamaño promedio de las células de Bacillus spp. tomadas 52 con TEM ÍNDICE DE FIGURAS Figura 1. Distribución espacial de bacterias aisladas del Sistema 25 Hidrológico Churince Figura 2. Variabilidad en la utilización de las diferentes fuentes de 36 carbono por los grupos taxonómicos de Bacillus spp Figura 3. Tasas de crecimiento máxima y densidad de saturación para 38 los diferentes grupos de Bacillus spp Figura 4. Rasgos de las cepas de los diferentes grupos taxonómicos 39 de Bacillus spp. Figura 5. Patrones de crecimiento y su relación con la producción de 41 “biofilm” Figura 6. Análisis de varianza de la frecuencia de esporulación de los 43 grupos taxonómicos de Bacillus spp Figura 7. Comparación del análisis filogenético entre los genes 16S 46 rRNA y gltX, y su asociación con la morfología. Figura 8. Crecimiento de cepas de Bacillus spp. en las diferentes 48 fuentes de fósforo. Figura 9. Imágenes de TEM de las cepas de Bacillus spp. 50 Figura 10. Imágenes TEM de B. horikoshii (A) y B. vietnamensis (B). 51 Figura 11. Análisis de MALDI-TOF de cepas de Bacillus spp. 53 relacionadas a ambientes acuáticos Figura 12. Análisis de MALDI-TOF de cepas de relacionadas a B. 54 cereus Figura 13. Espectros del grupo relacionado a B. thuringiensis 55 Figura 14. Análisis de MALDI-TOF de cepas de relacionadas a B. 56 subtilis Figura 15. Análisis de MALDI-TOF de cepas de relacionadas a B. 57 pumilus RESUMEN Numerosos trabajos han abordado la composición taxonómica de comunidades bacterianas de diferentes ambientes, pero se sabe poco con respecto a la variabilidad de los rasgos de los miembros de una comunidad. Aquí nos centramos en un solo género, en su mayor parte aislado de una comunidad de sedimento de una laguna extremadamente oligotrófica, y evaluamos rasgos fenotípicos conocidos por evolucionar en los extremos o puntas terminales y los que están profundamente enraizados en la filogenia, es decir, los rasgos recientemente adquiridos y los rasgos ancestrales. La muestra de estudio estuvo compuesta de 467 aislados del sistema acuático Churince ubicado en la Cuenca de Cuatrociénegas, Coahuila (Cuatro Cienegas Basin CCB), un sistema de agua que incluye una gran diversidad de grupos taxonómicos bien definidos de Bacillus spp. y que presentan una coherencia ecológica definida entre las comunidades de la muestra. La evaluación fenotípica de 141 aislados de Bacillus spp. de esta muestra reveló una gran variabilidad en todos los clados en los rasgos relacionados con la adquisición de compuestos de carbono, consistente con el intercambio de rasgos no complejos de las puntas terminales de la filogenia. Sin embargo, fue inesperada la alta variabilidad en los rasgos de linajes ancestrales y las notables diferencias específicas de clado, las auxotrofías fueron la norma en algunos clados. Dado que muchos de los rasgos evaluados pueden ser considerados rasgos de acción colectiva, como la motilidad, el “swarming”, la formación de “biofilm” y la utilización de fuentes de fósforo, futuros trabajos pueden revelar si la variabilidad observada es una manifestación de la evolución actuando a nivel individual o a nivel de la comunidad. 1 ABSTRACT Numerous works have addressed the taxonomic composition of bacterial communities from different environments, but little is known regarding the variability of traits in members of a community. Herein we focused on a single genus, isolated mostly from a sediment community in an extremely oligotrophic lagoon, and evaluated both phenotypic traits known to evolve at the tips and deeply enrooted in the phylogeny, that is, the newly acquired traits and ancestral traits. The sample under study was composed of 467 isolates from Churince at Cuatro Cienegas Basin (CCB), a water system that included a large diversity of well-defined taxonomic groups of Bacillus spp. and having a defined ecological coherence among the sampled communities. The phenotypic evaluation of 141 Bacillus spp. isolates from this sample revealed great variability in all clades in traits related to carbon compound acquisition, consistent with the exchange of non-complex traits at the tips of the phylogeny. It was unexpected, the high variability in ancestral lineages’ traits and the remarkable clade specific differences, auxotrophies were the norm in some clades. Since many of the evaluated traits can be considered collective action traits, such as swarming motility, biofilm formation and the use of phosphorus sources, it is intriguing whether the observed variability is a manifestation of evolution acting both at individual and community level. 2 1 INTRODUCCIÓN Las comunidades son ensamblajes de diferentes especies, en las cuales los organismos co-ocurren en un entorno determinado e interactúan unas con otras (Konopka, 2009). Las estrategias moleculares han sido fundamentales en el descubrimiento de la gran diversidad taxonómica de las comunidades microbianas.
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