Systems Biology and Synthetic Biology Laboratory

We are a multidisciplinary program that includes 7 researchers who routinely use a large number of approaches and experimental models. One of our main interests is to combine systems and synthetic biology using genome-scale models to design bacterial phenotypes of biotechnological interest (Dr. José Utrilla). In addition, we are also interested in using a theoretical-experimental approach to study the genetic and metabolic mechanisms that allow bacterial populations to find collective strategies to survive in hostile and unpredictable environments, such as antimicrobial substances (Dr. Rafael Peña). On the same vein, we also seek to understand the effects of spatial structure on the temporal dynamics of the evolution of bacterial resistance to different combinations of antibiotics (Dr. Ayari Fuentes). Additionally, we build a variety of evolutionary models to analyze specific genomic regions, such as the sex chromosomes, which are one of the most dynamic elements in the genomes of vertebrates. (Dr. Diego Cortez). Furthermore, using bacterial nitrogen fixation as an experimental model, we study the regulation of gene expression in response to various environmental stimuli and the mechanisms directing these responses (Dr. María de Lourdes Girard). We also study signal transduction and gene regulation in the genus Vibrio (Dr. David Zamorano). Finally, we analyze the metagenomics of the skin of amphibians and their interaction with pathogenic fungi (Dr. Eria Rebollar).

Group Staff

María de Lourdes Girard CuesyResearcherAssociate 3291686
Diego Cortez QuezadaResearcherAssociate 3291686
Ayari Fuentes HernándezResearcherAssistant 3291686
Marisa Rodríguez PadillaLaboratory TechnicianLaboratory 3291686
José Utrilla CarreriResearcherAssistant 3291686
Eria Rebollar CaudilloResearcherAssistant 3291686
David Salvador Zamorano SánchezResearcherAssistant 3291686
María de la Paz Elizabeth Salas OcampoLaboratory TechnicianLaboratory 3291686
Rafael Peña MillerResearcherAssociate 3291686
David Correa GaleotePostdoctoral 3175867

Group Publications

2018Chiozzotto, Remo, Ramirez, Mario, Talbi, Chouhra, Cominelli, Eleonora, Girard, Lourdes, Sparvoli, Francesca, Hernandez, Georgina (2018) Characterization of the Symbiotic Nitrogen-Fixing Common Bean Low Phytic Acid (lpa1) Mutant Response to Water Stress Genes 9(2):99- [doi:10.3390/genes9020099]29462877
2017Steffani-Vallejo, J.L., Zuñiga, C., Cruz-Morales, P., Lozano, L., Morales, M., Licona-Cassani, C., Revah, S., Utrilla, J. (2017) Draft Genome Sequence of Sphingobacterium sp. CZ-UAM, Isolated from a Methanotrophic Consortium. Genome announcements 5(33):e00792-17- [doi:10.1128/genomeA.00792-17]28818899
2017Moreno-Avitia, F., Lozano, L., Utrilla, J., Bolívar, F., Escalante, A. (2017) Draft Genome Sequence of Pseudomonas chlororaphis ATCC 9446, a Nonpathogenic Bacterium with Bioremediation and Industrial Potential. Genome announcements 5(23):e00474-17- [doi:10.1128/genomeA.00474-17]28596401
2017Utrilla, Jose (2017) Evolutionary Engineering of Microorganisms to Overcome Toxicity During Lignocellulose Hydrolysates Utilization Engineering of Microorganisms for the Production of Chemicals and Biofuels from Renewable Resources ():181-200 [doi:]
2017Vargas-Lagunas, Carmen, Mora, Yolanda, Diaz, Rafael, Martinez-Batallar, Gabriel, Girard, Lourdes, Encarnacion, Sergio, Peralta, Humberto, Mora, Jaime (2017) Overproduction of Sinorhizobium meliloti ArgC (N-acetyl-gamma-glutamyl phosphate reductase) promotes growth delay and inefficient nodules Fems Microbiology Letters 364(23):fnx233- [doi:10.1093/femsle/fnx233]29121239
2016Utrilla, Jose, Vargas-Tah, Alejandra, Trujillo-Martinez, Berenice, Gosset, Guillermo, Martinez, Alfredo (2016) Production of D-lactate from sugarcane bagasse and corn stover hydrolysates using metabolic engineered Escherichia coli strains BIORESOURCE TECHNOLOGY 220():208-214 [doi:10.1016/j.biortech.2016.08.067]27573474
2016Aguilar A, Peralta H, Mora Y, Díaz R, Vargas-Lagunas C, Girard L, Mora J (2016) Genomic Comparison of Agrobacterium pusense Strains Isolated from Bean Nodules Frontiers in Microbiology 7():1720-1720 [doi:10.3389/fmicb.2016.01720]27833604
2016Peralta H, Aguilar A, Díaz R, Mora Y, Martínez-Batallar G, Salazar E, Vargas-Lagunas C, Martínez E, Encarnación S, Girard L, Mora J (2016) Genomic studies of nitrogen-fixing rhizobial strains from Phaseolus vulgaris seeds and nodules Bmc Genomics 17():711-711 [doi:10.1186/s12864-016-3053-z]27601031
2016O'Brien EJ, Utrilla J, Palsson BO (2016) Quantification and Classification of E-coli Proteome Utilization and Unused Protein Costs across Environments Plos Computational Biology 12(6):e1004998- [doi:10.1371/journal.pcbi.1004998]27351952
2016Reyes-Gonzalez, Alma, Talbi, Chouhra, Rodriguez, Susana, Rivera, Patricia, Zamorano-Sanchez, David, Girard, Lourdes (2016) Expanding the regulatory network that controls nitrogen fixation in Sinorhizobium meliloti: elucidating the role of the two-component system hFixL-FxkR MICROBIOLOGY-SGM 162(6):979-988 [doi:10.1099/mic.0.000284]27010660
2016Utrilla, J., O'Brien, E.J., Chen, K., McCloskey, D., Cheung, J., Wang, H., Armenta-Medina, D., Feist, A.M., Palsson, B.O. (2016) Global Rebalancing of Cellular Resources by Pleiotropic Point Mutations Illustrates a Multi-scale Mechanism of Adaptive Evolution Cell systems 2(4):260-271 [doi:10.1016/j.cels.2016.04.003]27135538
2015Girard Cuesy, María de Lourdes, Zamorano Sánchez, David Salvador (2015) FNR - like proteins in rhizobia: past and future Biological Nitrogen Fixation 1():155-166 [doi:10.1002/9781119053095]
2015Nova-Franco B, Íñiguez LP, Valdés-López O, Alvarado-Affantranger X, Leija A, Fuentes SI, Ramírez M, Paul S, Reyes JL, Girard L, Hernández G (2015) The Micro-RNA172c-APETALA2-1 Node as a Key Regulator of the Common Bean-Rhizobium etli Nitrogen Fixation Symbiosis Plant Physiology 168(1):273-502 [doi:10.1104/pp.114.255547]25739700
2015Hernandez, Victor M., Girard, Lourdes, Hernandez-Lucas, Ismael, Vazquez, Alejandra, Ortiz-Ortiz, Catalina, Diaz, Rafael, Dunn, Michael F. (2015) Genetic and biochemical characterization of arginine biosynthesis in Sinorhizobium meliloti 1021 MICROBIOLOGY-SGM 161(8):1671-1682 [doi:10.1099/mic.0.000122]26271664
2014Mora, Yolanda, Diaz, Rafael, Vargas-Lagunas, Carmen, Peralta, Humberto, Guerrero, Gabriela, Aguilar, Alejandro, Encarnacion, Sergio, Girard, Lourdes, Mora, Jaime (2014) Nitrogen-Fixing Rhizobial Strains Isolated from Common Bean Seeds: Phylogeny, Physiology, and Genome Analysis Applied And Environmental Microbiology 80(18):5644-5654 [doi:10.1128/AEM.01491-14]25002426
2014Garcia-Garcia, J.D., Girard Cuesy, María de Lourdes, Hernández Delgado, Georgina, Saavedra, E., Pardo, J.P., Rodríguez-Zavala, J.S., Encalada, R., Reyes-Prieto, A., Mendoza-Cozatl, D.G., Moreno-Sánchez, R. (2014) Zn-bis-glutathionate is the best co-substrate of the monomeric phytochelatin synthase from the photosynthetic heavy metal-hyperaccumulator Euglena gracilis Metallomics 6(3):604-616 [doi:10.1039/c3mt00313b]24464102
2013Ramírez Yáñez, Mario, Guillén, G., Fuentes Membreño, Sara Isabel, Iñiguez Rabago, Luis Pedro, Aparicio Fabre, Rosaura, Zamorano Sánchez, David Salvador, Encarnación Guevara, Sergio Manuel, Panzeri, D., Castiglioni, B., Cremonesi, P., Strozzi, F., Stella, A., Girard Cuesy, María de Lourdes, Sparvoli, F., Hernández Delgado, Georgina (2013) Transcript profiling of common bean nodules subjected to oxidative stress Physiologia Plantarum 149(3):389-407 [doi:10.1111/ppl.12040]23432573
2013Ramírez Yáñez, Mario, Flores-Pacheco, G., Reyes, J.L., Álvarez, A.L., Drevon, J.J., Girard Cuesy, María de Lourdes, Hernández Delgado, Georgina (2013) Two Common Bean Genotypes with Contrasting Response to Phosphorus Deficiency Show Variations in the microRNA 399-Mediated PvPHO2 Regulation within the PvPHR1 Signaling Pathway International Journal Of Molecular Sciences 14(4):8328-8344 [doi:10.3390/ijms14048328]23591845
2013Aparicio Fabre, Rosaura, Guillén, G., Loredo, M., Arellano García, José de Jesús, Valdes López, Oswaldo, Ramírez Yáñez, Mario, Iñiguez Rabago, Luis Pedro, Panzeri, D., Castiglioni, B., Cremonesi, P., Strozzi, F., Stella, A., Girard Cuesy, María de Lourdes, Sparvoli, F., Hernández Delgado, Georgina (2013) Common bean (Phaseolus vulgaris L.) PvTIFY orchestrates global changes in transcript profile response to jasmonate and phosphorus deficiency Bmc Plant Biology 13():26-26 [doi:10.1186/1471-2229-13-26]23402340
2012Zamorano Sánchez, David Salvador, Reyes-González, A., Gómez Hernández, Nicolás, Rivera, P., Georgellis, D., Girard Cuesy, María de Lourdes (2012) FxkR Provides the Missing Link in the fixL-fixK Signal Transduction Cascade in Rhizobium etli CFN42 Molecular Plant-Microbe Interactions 25(11):1506-1517 [doi:10.1094/MPMI-05-12-0136-R]22809273
2012García-García, J.D., Olin-Sandoval, V., Saavedra, E., Girard Cuesy, María de Lourdes, Hernández Delgado, Georgina, Moreno-Sánchez, R. (2012) Sulfate uptake in photosynthetic Euglena gracilis. Mechanisms of regulation and contribution to cysteine homeostasis Biochimica Et Biophysica Acta-General Subjects 1820(10):1567-1575 [doi:10.1016/j.bbagen.2012.05.002]22609877
2012Talbi, C., Sánchez, C., Hidalgo-García, A., González, E.M., Arrese-Igor, C., Girard Cuesy, María de Lourdes, Bedmar, E.J., Delgado, M.J. (2012) Enhanced expression of Rhizobium etli cbb(3) oxidase improves drought tolerance of common bean symbiotic nitrogen fixation Journal Of Experimental Botany 63(14):5035-5043 [doi:10.1093/jxb/ers101]22511804
2011Cervantes de la Luz, Laura, Bustos Arcos, Virginia Patricia, Girard Cuesy, María de Lourdes, Santamaria Gutiérrez, Rosa Isela, Dávila Ramos, José Guillermo, Vinuesa Fleischmann, Pablo, Romero Camarena, David René, Brom Klanner, Susana (2011) The conjugative plasmid of a bean-nodulating Sinorhizobium fredii strain is assembled from sequences of two Rhizobium plasmids and the chromosome of a Sinorhizobium strain Bmc Microbiology 11(1):1-11 [doi:10.1186/1471-2180-11-149]21702991
2011Gómez Hernández, Nicolás, Reyes González, Alma Ruth, Sanchez, C., Pérez-Tejada Domínguez, Yolanda, Delgado, M.J., Girard Cuesy, María de Lourdes (2011) Regulation and Symbiotic Role of nirK and norC Expression in Rhizobium etli Molecular Plant-Microbe Interactions 24(2):233-245 [doi:10.1094/MPMI-07-10-0173]21043576
2011Díaz Mendez, Rafael, Vargas Lagunas, María del Carmen, Villalobos López, Miguel Angel, Peralta Díaz, Humberto, Pérez-Tejada Domínguez, Yolanda, Encarnación Guevara, Sergio Manuel, Girard Cuesy, María de Lourdes, Mora Celis, Jaime (2011) argC Orthologs from Rhizobiales Show Diverse Profiles of Transcriptional Efficiency and Functionality in Sinorhizobium meliloti Journal Of Bacteriology 193(2):460-472 [doi:10.1128/JB.01010-10]21075924
2010Talbi, C., Delgado, M. J., Girard, L., Ramirez-Trujillo, A., Caballero-Mellado, J., Bedmar, E. J. (2010) Burkholderia phymatum Strains Capable of Nodulating Phaseolus vulgaris Are Present in Moroccan Soils Applied And Environmental Microbiology 76(13):4587-4591 [doi:10.1128/AEM.02886-09]20472732
2010Sanchez, Cristina, Gates, Andrew J., Meakin, Georgina E., Uchiumi, Toshiki, Girard, Lourdes, Richardson, David J., Bedmar, Eulogio J., Delgado, Maria J. (2010) Production of Nitric Oxide and Nitrosylleghemoglobin Complexes in Soybean Nodules in Response to Flooding Molecular Plant-Microbe Interactions 23(5):702-711 [doi:10.1094/MPMI-23-5-0702]20367476
2010Talbi, C., Sánchez, C., Girard Cuesy, María de Lourdes, Bedmar, E., Delgado, M.J. (2010) La sobreexpresión de la oxidasa cbb3 de Rhizobium etli incrementa la tolerancia de Phaseolus vulgaris a la sequía Avances en el metabolismo del Nitrógeno ():223-228
2009Onofre-Lemus, Janette, Hernandez-Lucas, Ismael, Girard, Lourdes, Caballero-Mellado, Jesus (2009) ACC (1-Aminocyclopropane-1-Carboxylate) Deaminase Activity, a Widespread Trait in Burkholderia Species, and Its Growth-Promoting Effect on Tomato Plants Applied And Environmental Microbiology 75(20):6581-6590 [doi:10.1128/AEM.01240-09]19700546
2008Valdes-Lopez, Oswaldo, Arenas-Huertero, Catalina, Ramirez, Mario, Girard, Lourdes, Sanchez, Federico, Vance, Carroll P., Reyes, Jose Luis, Hernandez, Georgina (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots Plant Cell And Environment 31(12):1834-1843 [doi:10.1111/j.1365-3040.2008.01883.x]18771575
2008Vargas Lagunas, María del Carmen, Villalobos, M.A., Díaz Mendez, Rafael, Flores, M.A., Contreras Martínez, Sandra, Encarnación Guevara, Sergio Manuel, Pérez-Tejada Domínguez, Yolanda, Dunn, Michael Frederick, Girard Cuesy, María de Lourdes, Mora Celis, Jaime (2008) Comparative Analysis of ArgC protein expression in Rhizobium species Current Plant Science and Biotechnology. Agriculture Biological Nitrogen Fixation, Sustainable Agriculture and the Environment 42(0):239-240
2007Granados Baeza, Manuel Jesús, Gómez Hernández, Nicolás, Mora, Yolanda, Delgado, M.J., Romero Camarena, David René, Girard Cuesy, María de Lourdes (2007) Novel reiterated Fnr-type proteins control the production of the symbiotic terminal oxidase cbb(3) in Rhizobium etli CFN42 Molecular Plant-Microbe Interactions 20(10):1241-1249 [doi:10.1094/MPMI-20-10-1241]17918626
2007Flores López, Margarita, Morales Reyes, Lucía Guadalupe, Gonzaga Jáuregui, Claudia Gabriela, Domínguez Vidaña, Rocío, Zepeda Mendoza, Cinthya Jeanette, Yáñez Cuna, Jorge Omar, Gutiérrez Arcelus, María, Lemus Vergara, Tzitziki Janik, Valle García, David, Ávila Arcos, María del Carmen, Blanco Melo, Daniel, Medina Ruiz, Sofía, Meza Sosa, Karla Fabiola, Ayala Ortega, Erandi, García Alonso, Delfino, Bustos Arcos, Virginia Patricia, González Zúñiga, Víctor Manuel, Girard Cuesy, María de Lourdes, Tusie-Luna, T., Dávila Ramos, José Guillermo, Palacios de la Lama, Rafael (2007) Recurrent DNA inversion rearrangements in the human genome PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 104(15):6099-6106 [doi:10.1073/pnas.0701631104]17389356
2005Bueno, E., Gomez-Hernandez, Nicolas, Girard, L, Bedmar, E.J., Delgado, M.J. (2005) Function of the Rhizobium etli CFN42 nirK gene in nitrite metabolism BIOCHEMICAL SOCIETY TRANSACTIONS 33(1):162-163 [doi:10.1042/BST0330162]15667294
2005Vargas Lagunas, María del Carmen, Encarnación Guevara, Sergio Manuel, Girard Cuesy, María de Lourdes, Reyes Pérez, Agustín, Pérez-Tejada Domínguez, Yolanda, Mora Celis, Jaime (2005) Characterization of the alternative protection programs against oxidative-stress in free life and simbiosis from Rhizobium etli Current Plant Science and Biotechnology. Agriculture Biological Nitrogen Fixation, Sustainable Agriculture and the Environment 41():331-
2004Brom Klanner, Susana, Girard Cuesy, María de Lourdes, Tun Garrido, Cristina Soleda, García de los Santos, Alejandro, Bustos Arcos, Virginia Patricia, González Zúñiga, Víctor Manuel, Romero Camarena, David René (2004) Transfer of the symbiotic plasmid of Rhizobium etli CFN42 requires cointegration with p42a, which may be mediated by site-specific recombination Journal Of Bacteriology 186(22):7538-7548 [doi:10.1128/JB.186.22.7538-7548.2004]15516565
2004Vargas, M. del C., Encarnacin, S., Girard, M. de L., Reyes, A., Mora, Y., Mora, J. (2004) Physiological and proteome characterizations of oxidative-stress response in Rhizobium etli during free life and symbiosis with Phaseolus vulgaris. MOLECULAR & CELLULAR PROTEOMICS 3(10, S):160-160
2003González Zúñiga, Víctor Manuel, Bustos Arcos, Virginia Patricia, Ramírez Romero, Miguel Ángel, Medrano Soto, Luis Arturo, Salgado Osorio, Heladia, Hernández González, Ismael Luis, Hernández Celis, Juan Carlos, Quintero Hernández, Verónica, Moreno Hagelsieb, Gabriel, Girard Cuesy, María de Lourdes, Rodríguez Sánchez, Oscar, Flores López, Margarita, Cevallos Gaos, Miguel Ángel Carlos, Collado Vides, Pedro Julio, Romero Camarena, David René, Dávila Ramos, José Guillermo (2003) The mosaic structure of the symbiotic plasmid of Rhizobium etli CFN42 and its relation to other symbiotic genome compartments Genome Biology 4(6):R36- [doi:10.1186/gb-2003-4-6-r36]12801410
2002Brom Klanner, Susana, Girard Cuesy, María de Lourdes, García de los Santos, Alejandro, Sanjuan-Pinilla, J.M., Olivares, J., Sanjuan, J. (2002) Conservation of plasmid-encoded traits among bean-nodulating Rhizobium species Applied And Environmental Microbiology 68(5):2555-2561 [doi:10.1128/AEM.68.5.2555-2561-2002]11976134
2001López, O., Morera, C., Miranda-Ríos, J., Girard Cuesy, María de Lourdes, Romero Camarena, David René, Soberón Chávez, Mario (2001) Regulation of gene expression in response to oxygen in Rhizobium etli: Role of FnrN in fixNOQP expression and in symbiotic nitrogen fixation Journal Of Bacteriology 183(24):6999-7006 [doi:10.1128/JB.183.24.6999-7006.2001]11717256
2000Girard Cuesy, María de Lourdes, Brom Klanner, Susana, Dávalos Rodríguez, Araceli Elvira, López, O., Soberón Chávez, Mario, Romero Camarena, David René (2000) Differential regulation of fixN-reiterated genes in Rhizobium etli by a novel fixL-fixK-cascade Molecular Plant-Microbe Interactions 13(12):1283-1292 [doi:10.1094/MPMI.2000.13.12.1283]11106020
2000Reyes, J.D., Tabche, M.L., Morera, C., Girard Cuesy, María de Lourdes, Romero Camarena, David René, Krol, E., Miranda, J., Soberón Chávez, Mario (2000) Expression pattern of Rhizobium etli ccmIEFH genes involved in c-type cytochrome maturation Gene 250(1-2):149-157 [doi:10.1016/S0378-1119(00)00176-1]10854788
1999Soberon, M, Lopez, O, Morera, C, Girard, MD, Tabche, ML, Miranda, J (1999) Enhanced nitrogen fixation in a Rhizobium etli ntrC mutant that overproduces the Bradyrhizobium japonicum symbiotic terminal oxidase cbb(3) Applied And Environmental Microbiology 65(5):2015-201910223993
1998Flores, M, Mavingui, P, Girard, L, Perret, X, Broughton, WJ, Martinez-Romero, E, Davila, G, Palacios, R (1998) Three replicons of Rhizobium sp. strain NGR234 harbor symbiotic gene sequences Journal Of Bacteriology 180(22):6052-60539811668
1997RamirezRomero, MA, Bustos, P, Girard, L, Rodriguez, O, Cevallos, MA, Davila, G (1997) Sequence, localization and characteristics of the replicator region of the symbiotic plasmid of Rhizobium etli MICROBIOLOGY-SGM 143(8):2825-2831 [doi:10.1099/00221287-143-8-2825]9274036
1996Girard, L, Valderrama, B, Palacios, R, Romero, D, Davila, G (1996) Transcriptional activity of the symbiotic plasmid of Rhizobium etli is affected by different environmental conditions MICROBIOLOGY-SGM 142(10):2847-2856 [doi:10.1099/13500872-142-10-2847]
1996Valderrama, B, Davalos, A, Girard, L, Morett, E, Mora, J (1996) Regulatory proteins and cis-acting elements involved in the transcriptional control of Rhizobium etli reiterated nifH genes Journal Of Bacteriology 178(11):3119-3126 [doi:10.1128/jb.178.11.3119-3126.1996]8655489
1993Flores López, Margarita, Brom Klanner, Susana, Stepkowsky, Tomász, Girard Cuesy, María de Lourdes, Dávila Ramos, José Guillermo, Romero Camarena, David René, Palacios de la Lama, Rafael (1993) GENE AMPLIFICATION IN RHIZOBIUM - IDENTIFICATION AND INVIVO CLONING OF DISCRETE AMPLIFIABLE DNA REGIONS (AMPLICONS) FROM RHIZOBIUM-LEGUMINOSARUM BIOVAR PHASEOLI PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 90(11):4932-4936 [doi:10.1073/pnas.90.11.4932]8506337
1991GIRARD, MD, FLORES, M, BROM, S, ROMERO, D, PALACIOS, R, DAVILA, G (1991) STRUCTURAL COMPLEXITY OF THE SYMBIOTIC PLASMID OF RHIZOBIUM-LEGUMINOSARUM BV PHASEOLI Journal Of Bacteriology 173(8):2411-2419 [doi:10.1128/jb.173.8.2411-2419.1991]2013564
1985Quinto, Carmen, de la Vega, Humberto, Flores López, Margarita, Leemans, J., Cevallos Gaos, Miguel Ángel Carlos, Pardo Galván, Marco Aurelio, Azpiroz, Ricardo, Girard Cuesy, María de Lourdes, Calva Mercado, Edmundo, Palacios de la Lama, Rafael (1985) NITROGENASE REDUCTASE - A FUNCTIONAL MULTIGENE FAMILY IN RHIZOBIUM-PHASEOLI PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 82(4):1170-1174 [doi:10.1073/pnas.82.4.1170]16593543