Publications
2024
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Tibocha-Bonilla, J.D, Santibáñez-Palominos, R., Weng, Y., Kumar, M., Zengler. Proteome allocation of the microbiome reveals how diet and metabolic dysbiosis impact disease. bioRxiv doi.org/10.1101/2024.11.21.624724
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Neal, M., Brakewood, W., Betenbaugh, M., Zengler, K. Pan-genome metabolic modeling of Bacillus subtilis reveals functionally distrinct groups. mSystems e00923-24
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Aksenov, A.A., Blacutt, A., Ginnan, N., Rolshausen, P.E., Melnik, A.V., Lotfi, A., Gentry, E., Ramasamy, M., Zuniga, C., Zengler, K., Mandadi, K.K., Dorrestein, P.C, Roper, C., . Spatial chemistry of citrus reveals molecules bactericidal to Candidatus Liberibacter asiaticus. Scientific Reports 14, 20306.
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Lekbua, A., Thiruppathy, D., Coker, J., Weng, Y., Askarian, F., Kousha, A., Marotz, C., Hauw, A., Nizet, V., Zengler, K. SkinCom, a synthetic microbial community, enables reproducible investigations of the human skin microbiome. Cell Reports Methods 4:100832.
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Kumar, M., Tibocha-Bonilla, J.D., Füssy, Z., Lieng, C., Schwenck, S.M., Levesque, A.V., Al-Bassam, M.M., Passi, A., Neal, M., Zuniga, C., Kaiyom, F., Espinoza, J.L., Lim, H., Polson, S.W., Zeigler Allen, L., Zengler. K. Mixotrophic growth of a ubiquitous marine diatom. Science Advances 10:eado2623.
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Bunyavanich, S., Becker, P.M., Altman, M.C., Lasky-Su, J., Ober, C., Zengler, K., Berdyshev, E., Bonneau, R., Chatila, T., Chatterjee, N., Chung, K.F., Cutcliffe, C., Davidson, W., Dong, G., Fang, G., Fulkerson, P., Himes, B.E., Liang, L., Mathias, R.A., Ogino, S., Petrosino, J., Price, N.D., Schadt, E., Schofield, J., Seibold, M.A., Steen, H., Wheatley, L., Zhang, H., Togias, A., Hasegawa, K. Analytical challenges in omics research on asthma and allergy: a National Institute of Allergy and Infectious Diseases workshop. Journal of Allergy and Clinical Immunology https://doi.org/10.1016/j.jaci.2024.01.014.
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Gottel, N.R., Hill, M.S., Neal, M.J., Allard, S.M., Zengler, K., Gilbert, J.A. Biocontrol in built environments to reduce pathogen exposure and infection risk. ISME Journal https://doi.org/10.1093/ismejo/wrad024.
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Klapper, I., Szyld, D.B., Yu, X., Zengler, K., Zhang, T., Zuniga, C. A domain decomposition method for solution of a PDE-constrained generalized Nash equilibrium model of biofilm community metabolism. SIAM Journal on Applied Mathematics 84:97-113.
2023
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Neal, M., Thiruppathy, D., Zengler, K. Genome-scale metabolic modeling of the human gut bacterium Bacteroides fragilis strain 638R. PLoS Computational Biology https://doi.org/10.1371/journal.pcbi.1011594.
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Wang, B., Zuniga, C., Guernieri, M.T., Zengler, K., Betenbaugh, M., Young, J.D. Metabolic engineering of Synechococcus elongatus 7942 for enhanced sucrose biosynthesis. Metabolic Engineering 80:12-24.
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Tec-Campos, D., Posada, C., Tibocha-Bonilla, J.D., Thiruppathy, D., Glonek, N., Zuniga, C., Zepeda, A., Zengler, K. The genome-scale metabolic model for the purple non-sulfur bacterium Rhodopseudomonas palustris Bis A53 accurately predicts phenotypes under chemoheterotrophic, chemoautotrophic, photoheterotrophic, and photoautotrophic growth conditions. PLoS Computational Biology 19:e1011371.
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Moyne, O., Al-Bassam, M., Lieng, C., Thiruppathy, D., Norton, G.J., Kumar, M., Haddad, E., Zaramela, L.S., Zengler, K. Guild and niche determination enable targeted alteration of the microbiome. bioRxiv doi.org/10.1101/2023.05.11.540389.
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Li, C.-T., Eng, R., Zuniga, C., Hung, K.-W., Chen, Y., Zengler, K., Betenbaugh, M.J. Optimization of nutrient utilization efficiency and productivity for algal cultures under light and dark cycles using genome-scale model process control. npj Systems Biology and Applications 9:7.
2022
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Tibocha-Bonilla, J.D., Zuniga, C., Lekbua, A., Lloyd, C., Rychel, K., Short, K., Zengler, K. Predicting stress response and improved protein overproduction in Bacillus subtilis. npj Systems Biology and Applications 8:50.
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Coker, J., Zhalnina, K., Marotz, C., Thiruppathy, D., Tjuanta, M., D’Elia, G., Hailu, R., Mahosky, M., Rowan, M., Northen, T.R., Zengler, K. A reproducible and tunable synthetic soil microbial community provides new insights into microbial ecology. mSystems e00951-22.
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Tamasco, G., Kumar, M., Zengler, K., Silva-Rocha, R., da Silva, R.R. ChiMera: an easy to use pipeline for bacterial genome based metabolic network reconstruction, evaluation and visualization. BMC Bioinformatics 23:512.
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Zaramela, L.S., Tjuanta, M., Moyne, O., Neal, M., Zengler, K. synDNA – a synthetic DNA spike-in method for absolute quantification of shotgun metagenomic sequencing. mSystems e00447-22.
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Hakim, D., Wandro, S., Zengler, K., Zaramela, L.S., Nowinski, B., Swafford, A., Zhu, Q., Song, S.J., Gonzales, A., McDonald, D., Knight, R. Zebra: Static and dynamic genome cover thresholds with overlapping references. mSystems e00758-22.
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Hu, Y., Andeer, P.F., Zheng, Q., Kosina, S.M., Jardine, K.J., Ding, Y., Han, L.Z., Gao, Y., Zengler, K., Bowen, B.P., Mortimer, J.C., Vogel, J.P., Northen, T.R. Extensive plant use of exometabolites. bioRxiv doi: htpss://doi.org/10.1101/2022.07.29.496484.
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Martino, C., Zaramela, L.S., Gao, B., Embree, M., Tarasova, J., Parker, S.J., Wang, Y., Chu, H., Chen, P., Lee, K.-C., Domingos Galzerani, D., Gengatharan, J.M., Lekbua, A., Neal, M., Knight, R., Tsukamoto, H., Metallo, C., Schnabl, B., Zengler, K. Acetate reprograms gut microbiota during alcohol consumption. Nature Communications 13:4630.
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Severn, M.M., Williams, M.R., Shahbandi, A., Bunch, Z.L., Lyon, L.M., Nguyen, A., Zaramela, L.S., Todd D.A., Zengler, K., Cech, N.B., Gallo, R.L., Horswill, A.R. The ubiquitous human skin commensal Staphylococcus hominis protects against opportunistic pathogens. mBio 13:e00930.
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Salido, R.A., Martino, C., Karthikeyan, S., Huang, S., Rahman, G., Gonzalez, A., Zaramela, L.S., Beck, K.L., Bhute, S., Cantrell, K., Paola Carrieri, A. P., Farmer, S., Haiminen, N., Humphrey, G., Kim, H.-C., Parida, L., Richter, A., Vázquez-Baeza, Y., Zengler, K., Swafford, A.D., Bartko, A., Knight, R. Bacterial metatranscriptomes in wastewater can differentiate virally infected human population. bioRxiv doi: https://doi.org/10.1101/2022.02.23.481658.
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Canto-Encalada, G., Tec-Campos, D., Tibocha-Bonilla, J.D., Zengler, K., Zepeda, A., Zuniga, C. Flux balance analysis of the ammonia-oxidizing bacterium Nitrosomonas europaea ATCC19718 unravels specific metabolic activities while degrading toxic compounds. PLoS Computational Biology 18: https://doi.org/10.1371/journal.pcbi.1009828.
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Passi, A., Tibocha-Bonilla, J.D., Kumar, M., Tec-Campos, D., Zengler, K., Zuniga, C. Genome‐scale metabolic modeling enables in-depth understanding of big data. Metabolites 22:14.
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Coker, J., Zaramela, L.S., Zengler, K. Linking anaerobic gut bacteria and cardiovascular disease. Nature Microbiology 7:14-15.
2021
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Kawanishi, K., Coker, J.K., Grunddal, K.V., Dhar, C., Hsiao, J., Zengler, K., Varki, N., Varki, A., Gordts, P.L.S.M. Dietary Neu5Ac intervention protects against atherosclerosis associated with human-like Neu5Gc loss. Arteriosclerosis, Thrombosis, and Vascular Biology 41:2730-2739.
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Li, C.-T., Trigani, K., Zuniga, C., Eng, R., Chen, E., Zengler, K., Betenbaugh, M.J. Examining the impact of carbon dioxide levels and modulation of resulting hydrogen peroxide in Chlorella vulgaris. Algal Research 60:102492.
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Arnolds, K.L., Dahlin, L.R., Ding, L., Wu, C., Yu, J., Xiong, W., Zuniga, C., Suzuki, Y., Zengler, K., Linger, J.G., Guarnieri, M.T. Biotechnology for secure biocontainment designs in an emerging bioeconomy. Current Opinion in Biotechnology 71:25-31.
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Tibocha-Bonilla, J.D., Zuniga, C., Broddrick, J.T., Zengler, K., Godoy-Silva, R.D. A multiscale model predicts the sensitivity of Chlorella vulgaris to light and nitrogen levels in photobioreactors. bioRxiv doi.org/10.1101/2021.04.14.439858.
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Norena-Caro, D.A., Zuniga, C., Pete, A.J., Saemundsson, S.A., Donaldson, M.R., Adams, A.J., Dooley, K.M., Zengler, K., Benton, M.G. Analysis of the cyanobacterial amino acid metabolism with a precise genome-scale metabolic reconstruction of Anabaena sp. UTEX 2576. Biochemical Engineering Journal 171:108008.
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Zhou, R., Llorente, C., Cao, J., Zaramela, L.S., Zeng, S., Gao, B. Li, S.-Z., Welch, R.D., Huang, F.-Q., Qi, L.-W., Pan, C., Huang, Y., Zhou, P., Beussen, I., Zhang, Y., Byram, G., Fiehn, O., Wang, L., Lie, E.-H., Yu, R.T. Downes, M., Evans, R.M., Goglin, K., Fouts, D.E., Brenner, D.A., Bode, L., Fan, X., Zengler, K., Schnabl, B. Intestinal α1-2-fucosylation contributes to obesity and steatohepatitis in mice. Cellular and Molecular Gastroenterology and Hepatology 12:293-320.
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Sandoval, D.R., Clausen, T.M., Nora, C., Magida, J.A., Cribbs, A.P., Denardo, A., Clark, A.E., Garretson, A.F., Coker, J.K.C., Narayanan, A., Majowicz, S.A., Philpott, M., Johansson, C., Dunford, J.E., Spliid, C.B., Golden, G.J., Payne, N.C., Tye, M.A., Nowell, C.J., Griffis, E.R., Piermatteo, A., Grunddal, K.V., Alle, T., Hauser, B.M., Feldman, J., Caradonna, T.M., Pu, Y., Yin, X., McVicar, R.N., Kwong, E.M., Tsimikas, S., Schmidt, A.G., Ballatore, C., Zengler, K., Chanda, S.K., Weiss, R.J., Downes, M., Evans, R.M., Croker, B.A., Leibel, S.L., Jose, J., Mazitschek, R., Oppermann, U., Esko, J.D., Carlin, A.F., Gordts, P.L.S.M. 2021. The prolyl-tRNA synthetase inhibitor Halofuginone inhibits SARS-CoV-2 infection. bioRxiv doi:10.1101/2021.03.22.436522.
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Coker, J.K., Moyne, O., Rodionov, D., Zengler, K. Carbohydrates great and small, from dietary fiber to sialic acids: How glycans influence the gut microbiome and affect human health. Gut Microbes 13: e1869502
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Marotz, C., Morton, J.T., Navarro, P., Coker, J., Belda-Ferre, P., Knight, R., Zengler, K. Quantifying live microbial load in human saliva samples over time reveals stable composition and dynamic load. mSystems 6:e01182-20.
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Zaramela, L.S., Moyne, O., Kumar, M., Zuniga, C., Tibocha-Bonilla, J.D., Zengler, K. The sum is greater than the parts: Exploiting microbial communities to achieve complex functions. Current Opinion in Biotechnology 67: 149-157.
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Bali, P., Coker, J., Lozano-Pope, I., Zengler, K., Obonyo, M. Microbiome signatures in a fast- and slow-progressing gastric cancer murine model and their contribution to gastric carcinogenesis. Microorganisms 9: 189.
2020
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Allard, S.M., Costa, M.T., Bulseco, A.N., Helfer, V., Wilkins, L.G.E., Hassenruck, C., Zengler, K., Zimmer, M., Erazo, N., Mazza Rodrigues, J.L., Duke, N., Melo, V.M.M., Vanwonterghem, I., Junca, H., Makonde, H.M., Jimenez, D.J., Tavares, T.C.L., Fusi, M., Daffonchio, D., Duarte, C.M., Peixoto, R.S., Rosado, A.S., Gilbert, J.A., Bowman, J. Introducing the Mangrove Microbiome Initiative: identifying microbial research priorities and approaches to better understand, protect, and rehabilitate mangrove ecosystems. mSystems 5: e00658-20.
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Martino, C., Kellman, B.P., Sandoval, D.R., Clausen, T.M., Marotz, C.A., Song, S.J., Wandro, S., Zaramela, L.S., Salido Benitez, R.A., Zhu, Q., Armingol, E., Vazquez-Baeza, Y., McDonald, D., Sorrentino, J.T., Taylor, B., Belda-Ferre, P., Liang, C., Zhang, Y., Schifanella, L., Klatt, N.R., Havulinna, A.S., Jousilahti, P., Huang, S., Haiminen, N., Parida, L., Kim, H.C., Swafford, A.D., Zengler, K., Cheng, S., Inouye, M., Niiranen, T., Jain, M., Salomaa, V., Esko, J.D., Lewis, N.E., Knight, R. 2020. Bacterial modification of the host glycosaminoglycan heparan sulfate modulates SARS-CoV-2 infectivity. bioRxiv doi:10.1101/2020.08.17.238444.
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Zuniga, C., Peacock, B., Liang, B., McCollum, G., Irigoyen, S.C., Tec-Campos, D., Marotz, C., Weng, N.-C., Zepeda, A., Vidalakis, G., Mandadi, K.K., Borneman, J., Zengler, K. Linking metabolic phenotypes to pathogenic traits among ‘Candidatus Liberibacter asiaticus’ and its hosts. npj Systems Biology and Applications 6:24.
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Zuniga, C., Li, T., Guarnieri, M.T., Jenkins, J.P., Li, C.-T., Bingol, K., Kim, Y.-M., Betenbaugh, M.J., Zengler, K. Synthetic microbial communities of heterotrophs and phototrophs facilitate sustainable growth. Nature Communications 11: 3803.
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Tec-Campos, D., Zuniga, C., Passi, A., Del Toro, J., Tibocha-Bonilla, J.D., Zepeda, A., Betenbaugh, M.J., Zengler, K. Modeling of nitrogen fixation and polymer production in the heterotrophic diazotroph Azotobacter vinelandii DJ. Metabolic Engineering Communications 11.e00132.
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Sahoo, D., Zaramela, L.S., Hernandez, G.E., Mai, U., Taheri, S., Dang, D., Stouch, A.N., Medal, R.M., McCoy, A.M., Aschner, J.L., Blackwell, T.S., Zengler, K., Prince, L.S. Transcriptional profiling of lung macrophages identifies a predictive signature for inflammatory lung disease in preterm infants. Communications Biology 3:259.
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Tibocha-Bonilla, J.D., Kumar, M., Richelle, A., Godoy-Silva, R.D., Zengler, K., Zuniga, C. Dynamic resource allocation drives growth under nitrogen starvation in eukaryotes. npj Systems Biology and Applications 6:14.
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Al-Bassam, M.M., Moyne, O., Chapin, N., Zengler, K. Nucleoid openness profiling links bacterial genome structure to phenotype. bioRxiv doi.org/10.1101/2020.05.07.082990.
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Liu, Y.F., Chen, J., Zaramela, L.S., Wang, L.-Y., Mbadinga, S.M., Hou, Z.-W., Wu, X.-L., Gu, J-G., Zengler, K. Mu, B.-Z. Genomic and transcriptomic evidence supports methane metabolism in Archaeoglobi. mSystems 5:e00651-19.
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Williams, M.R., Cau, L., Wang, Y., Kaul, D., Sanford, J.A., Zaramela, L.S., Khalil, S., Butcher, A., Zengler, K., Hoswill, A.R., Dupont, C.L., Hovnanian, A., Gallo, R.L. Interplay of staphylococcal and host proteases promotes skin barrier disruption in Netherton Syndrome. Cell Reports 30:2923-2933 e7.
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Jun Xu, J., Ma, H.-Y, Liu, X, Rosenthal, S., Baglieri, J., McCubbin, R., Sun, M., Koyama, Y., Geoffroy, C.G., Saijo, K., Shang, L., Nihoshi, T., Maricic, I., Kreifeldt, M., Kusumanchi, P., Roberts, A., Zheng, B., Kumar, V., Zengler, K., Pizzo, D.P., Hosseini, M., Contet, C., Glass, C.K., Liangpunsakul, S., Tsukamoto, H., Gao, B., Karin, M., Brenner, D.A., Koob, G.F., Kisseleva, T. Blockade of lL-17A signaling reverses alcohol-induced liver injury and excessive alcohol drinking in mice. JCI Insight 5:e131277.
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Li, T., Jiang, L., Hu, Y., Jackson, P., Zuniga, C., Zengler, K. Betenbaugh, M.J. Creating a synthetic lichen: Mutualistic co-culture of fungi and extracellular polysaccharide-secreting cyanobacterium Nostoc PCC 7413. Algal Research 45:101755.
2019
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Zuniga, C., Li, C.-T., Yu, G., Al-Bassam, M.M., Li, T.-T., Jiang, L., Zaramela, L.S., Guarnieri, M., Betenbaugh, M.J., Zengler, K. Environmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communities. Nature Microbiology 4:2184–2191.
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Zaramela, L.S., Martino, C., Alisson-Silva, F., Rees, S.D., Diaz, S.L., Chuzel, L., Ganatra, M.B., Taron, C.H., Secrest, P., Zuniga, C., Huang, J., Chang, G., Varki, A., Zengler, K. Gut bacteria responding to dietary change encode sialidases that exhibit preference for red meat-associated carbohydrates. Nature Microbiology 4:2082-2089.
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Li, C.-T., Yelsky, J., Chen, Y., Zuniga, C., Eng, R., Jiang, L., Shapiro, A., Huang, K.-W., Zengler, K., Betenbaugh, M.J. A model predictive control strategy utilizing genome-scale models to optimize nutrient supply for sustained algal growth and lipid productivity. npj Systems Biology and Applications 5:33.
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Gao, N.J., Al-Bassam, M.M., Poudel, S., Wozniak, J.M., Gonzalez, D.J., Olson, J., Zengler, K., Nizet, V. Valderrama, J.A. Functional and proteomic analysis of Streptococcus pyogenes virulence upon loss of its native Cas9 nuclease Frontiers in Microbiology 10:1967.
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Kumar, M., Ji, B., Zengler, K., Nielsen, J. Modelling approaches for studying the microbiome. Nature Microbiology 4:1253-1267.
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Zengler, K., Hofmockel, K., Baliga, N.S., Behie, S.W., Bernstein, H.C., Brown, J.B., Dinneny, J.R., Floge, S.A., Forry, S.P., Hess, M., Jackson, S.A., Jansson, C., Lindemann, S.R., Pett-Ridge, J., Maranas, C., Venturelli, O.S., Wallenstein, M.D., Shank, E.A., Northen, T. EcoFAB: Advancing microbiome science through standardized fabricated ecosystems. Nature Methods 16:567-571.
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Morton, J.T., Martoz, C., Silverman, J., Washburne, A., Zaramela, L.S., Edlund, A., Zengler, K.*, Knight, R.* Establishing microbial measurement standards with reference frames. Nature Communications 10:2719.
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Bouslimani, A., da Silva, R. Kosciolek, T., Janssen, S., Callenwaert, C., Amir, A., Dorrestein, K., Melnik, A.V., Zaramela, L.S., Kim, J.-N., Humphrey, G., Schwartz, T., Sanders, K., Brennan, C., Luzzatto-Knaan, T., Ackermann, G., McDonald, D., Zengler, K., Knight, R., Dorrestein, P.C. The impact of skin care products on skin chemistry and microbiome. BMC Biology 17:47.
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Williams, M.R., Costa, S.K., Zaramela, L.S., Khalil, S., Todd, D.A., Winter, H.L., Sanford, J.A., O’Neill, A.M., Liggins, M.C., Nakatsuji, T., Cech, N.B., Cheung, A.L., Zengler, K., Horswill, A.R., Gallo, R.L. Quorum sensing between bacterial species on the skin protects against epidermal injury in atopic dermatitis. Science Translational Medicine 11:eaat8329.
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Wu, C.-C., Kim, J.-N., Wang, Z., Chang, Y.-L., Zengler, K., Di Nardo, A. Mast cell recruitment is modulated by hairless skin microbiome. Journal of Allergy and Clinical Immunology 144:330-333.
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Liu, J.K., Lloyd, C., Al-Bassam, M.M., Ebrahim, A., Kim, J.-K., Olson, C., Aksenov, A., Dorrestein, P., Zengler, K. Predicting proteome allocation, overflow metabolism, and metal requirements in a model acetogen. PLoS Computational Biology 15: e1006848.
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Leung, D.Y.M., Calatroni, A., Zaramela, L.S., LeBeau, P.K., Dyjack, N., Brar, K., David, G., Johnson, K., Leung, S., Ramirez-Gama, M., Liang, B., Rios, C., Montgomery, M.T., Richers, B.N., Hall, C.F., Norquest, K.A., Jung, J., Bronova, I., Kreimer, S., Talbot Jr., C.C., Crumrine, D., Cole, R.N., Elias, P., Zengler, K., Seibold, M.A., Berdyshev, E., Goleva, E. The non-lesional skin surface distinguishes atopic dermatitis with food allergy as a unique endotype. Science Translational Medicine 11:eaav2685.
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Martino, C., Morton, J.T., Marotz, C.A., Thompson, L.R., Tripathi, A., Knight, R. Zengler, K. A novel sparse compositional technique reveals microbial perturbations. mSystems 4:e00016-19.
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Shin, B., Kim, M., Zengler, K., Chin, K.-J., Overholt, W.A., Gieg, L.M., Konstantinidis, K.T., Kostka, J.E. Anaerobic degradation of hexadecane and phenanthrene coupled to sulfate reduction by enriched consortia from northern Gulf of Mexico seafloor sediment. Scientific Reports 9:1239.
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Seif, Y., Monk, J.M., Mih, N., Tsunemoto, H., Poudel, S., Zuniga, C., Broddrick, J., Zengler, K., Palsson, B.O. A multi-scale computational knowledge-base for Staphylococcus aureus elucidates the response to different media types. PLoS Computational Biology 15:e1006644.
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Strandwitz, P., Kim, K.H., Terekhova, D., Liu, J.K., Sharma, A., Levering, J., McDonald, D., Dietrich, D., Ramadhar, T.R., Lekbua, A., Mroue, N., Liston, C., Stewart, E.J., Dubin, M.J., Zengler, K., Knight, R., Gilbert, J.A., Clardy, J., Lewis, K. GABA-modulating bacteria of the human gut microbiota. Nature Microbiology 4:396-403.
2018
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Al-Bassam, M.M., Kim, J.-N., Zaramela, L.S., Kellman, B.P., Zuniga, C., Wozniak, J.M., Gonzalez, D.J., Zengler, K. Optimization of carbon and energy utilization through differential translational efficiency. Nature Communications 9:4474.
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Tibocha-Bonilla, J.D., Zuniga, C., Godoy-Silva, R.D., Zengler, K. Advances in metabolic modeling of oleaginous microalgae. Biotechnology for Biofuels 11:241.
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Zhalnina, K., Zengler, K., Newman, D., Northen, T.R. Need for laboratory ecosystems to unravel the structures and functions of soil microbial communities mediated by chemistry. mBio 9:e01175-18.
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Patras, K.A., Derieux, J., Al-Bassam, M.M., Adiletta, N., Vrbanac, A., Lapek, J.D., Zengler, K., Gonzalez, D.J., Nizet, V. Group B Streptococcus biofilm regulatory protein A contributes to bacterial physiology and innate immune resistance. Journal of Infectious Diseases 218:1641-1652.
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McDonald et al. American Gut: an open platform for citizen-science microbiome research. mSystems 3:e00031-18.
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Latif, H., Federowicz, S., Ebrahim, A., Tarasova, J., Szubin, R., Utrilla, J., Zengler, K., Palsson, B.O. ChIP-exo interrogation of Crp, DNA, and RNAP holoenzyme interactions. PLoS One 13: e0197272.
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Zengler, K. & Zaramela, L.S. The social network of microorganisms - how auxotrophies shape complex communities. Nature Reviews Microbiology 16:383-390. Journal Cover
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Guarnieri, M.T., Levering, J., Henard, C.A., Boore, J., Betenbaugh, M., Zengler, K., Knoshaug, E. Genome sequence of the oleaginous green alga, Chlorella vulgaris UTEX 395. Frontiers in Bioengineering and Biotechnology 6:37.
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Marotz, C.A., Sanders, J.G., Zuniga, C., Zaramela, L.S., Knight, R., Zengler, K. Improving saliva shotgun metagenomics by chemical host DNA depletion. Microbiome 6:42.
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McDonald et al. American Gut: an open platform for citizen-science microbiome research. bioRxiv doi.org/10.1101/277970.
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Behrendt, L., Shah, S.A., Zengler, K., Sørensen, S.J., Lindorff-Larsen, K., Winther, J.R. Deep mutational scanning by FACS-sorting of encapsulated E. coli micro-colonies. bioRxiv doi.org/10.1101/274753.
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Bluemel, S., Wang, L., Martino, C., Lee, S., Willliams, B., Horvath, A., Stadlbauer, V., Zengler, K., Schnabl, B. The role of intestinal Reg3 lectins for non-alcoholic steatohepatitis. Hepatology Communications 2:393-406.
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Liu, Y., Domingos Galzerani, D., Mbadinga, S.M., Zaramela, L.S., Gu, J., Mu, B., Zengler, K. Metabolic capability and in situ activity of microorganisms in an oil reservoir. Microbiome 6:5.
2017
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Zuniga, C., Levering, J., Antoniewicz, M.R., Guarnieri, M.T., Betenbaugh, M.J., Zengler, K. Predicting dynamic metabolic demands in the photosynthetic eukaryote Chlorella vulgaris. Plant Physiology 176:450-462.
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Zuniga, C., Zaramela, L., Zengler, K. Elucidation of complexity and prediction of interactions in microbial communities. Microbial Biotechnology 10:1500-1522.
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Wankel, S.D., Ziebis, W., Buchwald, C., Charoenpong, C., de Beer, D., Dentinger, J., Xu, Z., Zengler, K. Evidence for fungal chemodenitrification based N2O flux from nitrogen impacted coastal sediments. Nature Communications 8:15595.
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Nakatsuji, T., Chen, T.H., Narala, S., Chun, K.A., Two, A.M., Yun, T., Shafiq, F., Kotol, P.F., Bouslimani, A., Melnik, A.V., Latif, H., Kim, J.-N., Artis, A.L.K., David, G., Taylor, P., Streib, J., Dorrestein, P.C., Grier, A., Gill, S.R., Zengler, K., Hata, T.R., Leung, D.Y.M., Gallo, R.L. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Science Translational Medicine 9:eaah4680.
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Levering, J., Dupont, C., Allen, A., Palsson, B., Zengler, K. Integrated regulatory and metabolic network of the marine diatom Phaeodactylum tricornutum predicts the response to rising CO2 levels. mSystems 2:e00142-16. Editor's Pick
2016
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Latif, H., Federowicz, S., Ebrahim, A., Tarasova, J., Szubin, R., Utrilla, J., Zengler, K., Palsson, B.O. ChIP-exo interrogation of Crp, DNA, and RNAP holoenzyme interactions. bioRxiv doi: http://dx.doi.org/10.1101/069021.
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Zengler, K. Overview of the skin microbiome - Commented Bibliographies. FRT - Fondation Rene Touraine. Experimental Dermatology 25:918-919.
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Zuniga, C., Li, C.-T., Huelsman, T., Levering, J., Zielinski, D.C., McConnell, B.O., Long, C.P., Knoshaug, E.P., Guarnieri, M.T., Antoniewicz, M.R., Betenbaugh, M.J., Zengler, K. Genome-scale metabolic model for the green alga Chlorella vulgaris UTEX 395 accurately predicts phenotypes under autotrophic, heterotrophic, and mixotrophic growth conditions. Plant Physiology 172:589-602.
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Gallina, A.A., Layer, M., King, Z., Levering, J., Palsson, B.O., Zengler, K.*, Peers, G. A* Phaeodactylum tricornutum literature database for interactive annotation of content. Algal Research 18:241-243.
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Movahedi, N.S., Embree, M., Nagarajan, H., Zengler, K., Chitsaz, H. Efficient synergistic single-cell genome assembly. Frontiers in Bioengineering 4:42.
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Levering, J., Broddrick, J. Dupont, C., Peers, G., Beeri, K., Mayers, J., Gallina, A.A., Allen, A., Palsson, B., Zengler, K. Genome-scale model reveals metabolic basis of biomass partitioning in a model diatom. PLoS One 11(5):e0155038. 2016. Top 25% most cited articles of 2016
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Faraghiparapari, N. & Zengler, K. Production of organics from CO2 by microbial electrosynthesis (MES) at high temperature. Journal of Chemical Technology & Biotechnology 92:375-381.
2015
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Embree, M., Liu, J., Al-Bassam, M.M., Zengler, K. Networks of energetic and metabolic interactions define dynamics in microbial communities. Proceedings of the National Academy of Science, U.S.A. 112:15450-15455.
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Levering, J., Broddrick, J., Zengler, K. Engineering of oleaginous organisms for lipid production. Current Opinion in Biotechnology, 36:32-39.
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Latif, H., Sahin, M., Tarasova, J., Tarasova, Y., Portnoy, V.A., Zengler, K. Adaptive evolution of Thermotoga maritima reveals plasticity of the ABC transporter network. Applied and Environmental Microbiology 81:5477-5485. Highlighted by Faculty of 1000
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Islam, M.A., Zengler, K., Edwards, E.A., Mahadevan, R., Stephanopoulos, G. Investigating Moorella thermoacetica metabolism with a genome-scale constraint-based metabolic model. Integrative Biology 7:869-882.
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Latif, H., Szubin, R., Tan, J., Brunk, E., Lechner, A., Zengler, K.*, Palsson, B.O. A streamlined ribosome profiling protocol for the characterization of microorganisms. BioTechniques 58:329-332.
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Tan, J., Zuniga, C., Zengler, K. Unraveling interactions in microbial communities - from co-cultures to microbiomes. Journal of Microbiology 53:295-305.
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Patil, S.A., Gildemyn, S., Pant, D., Zengler, K., Logan, B.E., Rabaey, K. A logical data representation framework for electricity-driven bioproduction processes. Biotechnology Advances 33:736-744.
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Chen, P., Torralba, M., Tan, J., Embree, M., Zengler, K., Stärkel, P., van Pijkeren, J.-P., DePew, J., Loomba, R., Ho, S.B., Bajaj, J.S., Mutlu, E.A., Keshavarzian, A., Tsukamoto, H., Nelson, K.E., Fouts, D.E., Schnabl, B. Supplementation of saturated long-chain fatty acids maintains intestinal eubiosis and reduces ethanol-induced liver injury in mice. Gastroenterology 148:203-214.
2014
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Rotaru, A.E., Shrestha, P.M., Liu, F., Shrestha, D., Wardmann, C., Embree, M., Zengler, K. Nevin, K.P., Lovley, D.R. A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy and Environmental Science 7:408-415.
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Latif, H., Zeidan, A., Nielsen, A. T., Zengler, K. Trash to treasure: Production of biofuels and commodity chemicals via syngas fermenting microorganisms. Current Opinion in Biotechnology 27:79-87.
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Cho, B.-K., Kim, D., Knight, E.M., Zengler, K., Palsson, B.O. Genome-scale reconstruction of the sigma factor network in Escherichia coli: topology and functional states. BMC Biology 12:4.
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Federowicz, S., Kim, D., Ebrahim, A., Lerman, J., Nagarajan, H., Zengler, K., Cho, B.-K., Palsson, B.O. Determining the control circuitry of redox metabolism at the genome-scale. PLoS Genetics 10:e1004264.
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Embree, M., Qiu, Y., Shieu, W., Nagarajan, H., O’Neil, R., Lovley, D.R., Zengler, K. The Fur regulon of Geobacter sulfurreducens and its role in energy metabolism. Applied and Environmental Microbiology 80:2918-2927.
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Feist, A.M., Nagarajan, H., Rotaru, A.-E., Tremblay, P.-L., Zhang, T., Nevin, K.P., Lovley, D.R., Zengler, K. Constraint-based modeling of carbon fixation and the energetics of external electron transfer in Geobacter metallireducens GS-15. PLoS Computational Biology 10:e1003575.
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Liu, J.K., O’Brien, E.J., Lerman, J.A., Zengler, K., Palsson, B.O., Feist, A.M. Reconstruction and modeling protein translocation and compartmentalization in Escherichia coli at the genome-scale. BMC Systems Biology 8:110. Editor's Pick
2013
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Gong, Y., Ebrahim, A., Feist, A.M., Embree, M., Zhang, T., Lovley, D.R., Zengler, K. Sulfide-driven microbial electrosynthesis. Environmental Science & Technology 47:568-573.
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Curtis, T., Daran, J.-M., Pronk, J.T., Frey, J., Jansson, J.K., Robbins-Pianka, A., Knight, R., Schnürer, A., Smets, B.F., Smid, E.J., Abee, T., Vicente, M., Zengler, K. I C1 C1-Future. Crystal ball – 2013. Microbial Biotechnology 6:3-16.
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Nakatsuji, T., Jian, S.B., Chiang, H.-I., Zengler, K., Gallo, R.L. The microbiome extends to subepidermal compartments of normal skin. Nature Communications 4:1431.
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Qiu, Y., Nagarajan, H., Embree, M. Shieu, Abate, E., Juárez, K., Cho, B.-K., Elkins, J., Nevin, K.P., Barrett, C.L., Lovley, D.R., Palsson, B.O., Zengler, K. Characterizing the interplay between multiple levels of organization within bacterial sigma factor regulatory networks. Nature Communications 4: 1755.
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Latif, H., Lerman, J.A., Portnoy, V.A., Tarasova, Y., Nagarajan, H., Schrimpe-Rutledge, A.C., Smith, R.D., Adkins, J.N., Lee, D.H., Qiu, Y., Zengler, K. The genome organization of Thermotoga maritima reflects its lifestyle. PLoS Genetics 9:e1003485. Highlighted by Faculty of 1000
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Rodionov, D.A., Rodionova, I.A., Li, X., Ravcheev, D.A., Tarasova, Y., Portnoy, V.A., Zengler, K., Osterman, A.L. Transcriptional regulation of carbohydrate utilization network in Thermotoga maritima. Frontiers in Microbiology 4:244.
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Movahedi, N.S., Taghavi, Z., Embree, M., Nagarajan, H., Zengler, K., Chitsaz, H. Efficient syngergistic single-cell genome assembly. bioRxiv. doi: https://doi.org/10.1101/002972.
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Embree, M., Nagarajan, H., Movahedi, N., Chitsaz, H., Zengler, K. Single cell genome and metatranscriptome sequencing reveal the metabolic capabilities and interspecies interactions of a alkane-degrading methanogenic community. ISME Journal 8:757-767. 2014.
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Nagarajan, H., Embree, M. Rotaru, A.-E., Shrestha, P.M., Feist, A.M., Palsson, B.O., Lovley, D.R., Zengler, K.Characterization of interspecies electron transfer mechanisms and microbial community dynamics of a syntrophic association. Nature Communications 4:2809. Highlighted by Nature Reviews Microbiology
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Nagarajan, H., Sahin, M., Nogales, J., Latif, H., Lovley, D.R., Ebrahim, A., Zengler, K. Characterizing acetogenic metabolism using a genome-scale metabolic reconstruction of Clostridium ljungdahlii. Microbial Cell Factories 12:118. Highly Accessed Article
2012
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Cho, B.-K., Federowicz, S.A, Park, Y.S., Zengler, K., Palsson, B.O. Deciphering the transcriptional regulatory logic of amino acid metabolism. Nature Chemical Biology 8:65-71.
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Ravcheev, D.A., Li, X., Portnoy, V.A., Zengler, K., Osterman, A.L., Rodionov, D.A. Transcriptional regulation of hydrogen production and central metabolism in Thermotoga maritima by a redox-responsive Rex-family repressor. Journal of Bacteriology 194:1145-1157.
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Zengler, K. & Palsson, B.O. A road map for the development of community systems (CoSy) biology. Nature Reviews Microbiology 10:366-372. Journal Cover
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Lerman, J.A., Hyduke, D.R., Latif, H., Portnoy, V.A., Lewis, N.E., Orth, J.D., Schrimpe-Rutledge, A.C., Smith, R.D., Adkins, J.N., Zengler, K., Palsson, B.O. In silico method for modeling metabolism and gene product expression at genome scale. Nature Communications 3:929.
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Alain, K., Harder, J., Widdel, F., Zengler, K. Anaerobic utilization of toluene by marine Alpha- and Gammaproteobacteria reducing nitrate. Microbiology 158:2946-2957.
2011
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Thiele, I., Hyduke, D., Steeb, B., Fankam, G., Allen, D.K., Bazzani, S., Charusanti, P., Chen, F.-C., Fleming, R.M.T., Hsiung, C.A., De Keersmaecker, S.C.J., Liao, Y.-C., Marchal, K., Mo, M.L., Özdemir, E., Raghunathan, A., Reed, J.L., Shin, S.-I., Sigurbjörnsdóttir, S., Steinmann, J., Sudarsan, S., Swainston, N., Thijs, I.M., Zengler, K., Palsson, B.O., Adkins, J.N., Bumann, D. A community effort towards a knowledge-base and mathematical model of the human pathogen Salmonella Typhimurium LT2. BMC Systems Biology 5:8.
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Portnoy, V.A., Bezdan, D., Zengler, K. Adaptive laboratory evolution – Harnessing the power of biology for metabolic engineering. Current Opinion in Biotechnology 22:590-594.
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Cho, B.-K., Palsson, B.O., Zengler, K. Deciphering the regulatory codes in bacterial genomes. Biotechnology Journal 6:1052-1063.
2010
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Feisthauer, S., Siegert, M., Seidel, M., Richnow, H.H., Zengler, K., Gründger, F., Krüger, M. Isotopic fingerprinting of methane and CO2 formation from aliphatic and aromatic hydrocarbons. Organic Geochemistry 41:482-490.
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Nagarajan, H., Butler, J., Klimes, A., Qiu, Y., Zengler, K., Methe, B.A., Palsson, B.O., Lovley, D.R., Barrett, C.L. De novo assembly of a complete microbial genome using short reads: The case of an enhanced electricity-producing variant of Geobacter sulfurreducens. PLoS One 5:e10922.
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Qiu, Y., Cho, B.-K., Park, Y.S., Lovley, D., Palsson, P.O., Zengler, K. Structural and operational complexity of the Geobacter sulfurreducens genome. Genome Research 20:1304-1311.
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Tremblay, P.L., Summers Z.M., Glaven R.H., Nevin K.P., Zengler K., Barrett C.L., Qiu Y., Palsson B.O., Lovley, D.R. A c-type cytochrome and a transcriptional regulator responsible for enhanced extracellular electron transfer in Geobacter sulfurreducens revealed by adaptive evolution. Environmental Microbiology 13:13-23.
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Klimes, A., Franks, A.E., Glaven, R.H., Tran, H., Barrett, C.L., Qiu, Y., Zengler, K., Lovley, D.R. Production of pilus-like filaments in Geobacter sulfurreducens in the absence of the type IV pilin protein PilA. FEMS Microbiology Letters 310:62-68.
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Palsson, B.O. & Zengler, K. The challenge of integrating multi-omic data sets. Nature Chemical Biology 6: 787-789.
2009
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Cho, B.-K., Zengler, K., Qiu, Y., Park, Y.S., Knight, E.M., Barrett, C., Gao, Y., Palsson, B.O. Elucidation of the transcription unit architecture of the Escherichia coli K-12 MG1655 genome. Nature Biotechnology 27:1043-1049. Journal Cover
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Zengler, K. The central role of the cell in microbial ecology. Microbiology and Molecular Biology Reviews 73:712-729.
2007
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Podar, M., Abulencia, C., Walcher, M., Hutchinson, D., Zengler, K., Garcia, J., Holland, T., Cotton, D., Hauser, L., Keller, M. Targeted access to the genomes of low abundance organisms in complex microbial communities. Applied and Environmental Microbiology 73:3205-3214.
2005
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Vadim, V.K., Zengler, K., Lysenko, A.M., Wiegel, J. Anoxybacillus kamchatkensis sp. nov., a novel thermophilic facultative aerobic bacterium with a broad pH optimum from the Geyser valley, Kamchatka. Extremophiles 9:391-398.
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Zengler, K., Walcher, M., Clark, G., Toledo, G., Haller, I., Holland, T., Mathur, E.J., Woodnutt, G., Short, J.M., Keller, M. High throughput cultivation of oligotrophic microorganisms. In: Leadbetter, J.R. (ed) Methods in Enzymology 397:124-130.
2004
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Keller, M. & Zengler, K. Tapping into microbial diversity. Nature Reviews Microbiology 2:141-150.
2002
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Zengler, K., Toledo, G., Rappé, M., Elkins, J., Mathur, E.J., Short, J.M., Keller, M. Cultivating the uncultured. Proceedings of the National Academy of Science, U.S.A. 99:15681-15686. Highlighted by Faculty of 1000
2000
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Wilkes, H., Boreham, C., Harms, G., Zengler, K., Rabus, R. Anaerobic degradation and carbon isotopic fractionation of alkylbenzenes in crude oil by sulphate-reducing bacteria. Organic Geochemistry 21:101-115.
1999
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Zengler, K., Heider, J., Rosselló-Mora, R., Widdel, F. Phototrophic utilization of toluene under anoxic conditions by a new strain of Blastochloris sulfoviridis. Archives of Microbiology 172:204-212.
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Harms, G., Zengler, K., Rabus, R., Aeckersberg, F., Minz, D., Rosselló-Mora, R., Widdel, F. Anaerobic oxidation ofo‑xylene, m‑xylene, and homologous alkylbenzenes by new types of sulfate-reducing bacteria. Applied and Environmental Microbiology 65:999-1004. First two authors contributed equally to the work.
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Champion, K.M., Zengler, K., Rabus, R. Anaerobic degradation of ethylbenzene and toluene in denitrifying strain EbN1 proceeds via independent substrate-induced pathways. Journal of Molecular Microbiology and Biotechnology 1:157-164.
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Zengler, K., Richnow, H.H., Rosselló-Mora, R., Michaelis, W., Widdel, F. Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401:266-269. Nature News and Views
BOOK CHAPTERS
BOOK CHAPTERS
BOOK CHAPTERS
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Tibocha-Bonilla, J.D., Kumar, M., Zengler, K., Zuniga, C. Integrating metabolic modeling and high-throughput data to characterize diatoms metabolism. In: Pappas, J.L. (ed) The Mathematical Biology of Diatoms. Scrivener Publishing LLC, Beverly, MA, p.165-191. 2023.
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Al-Bassam, M.M. & Zengler, K. Determination of the chromatin openness in bacterial genomes. In: Marinov, G.K., Greenleaf, W.J. (eds) Chromatin Accessibility. Methods in Molecular Biology. vol 2611.Humana Press, New York, NY, p.63-69. 2023.
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Kumar, M., Zuniga, C. Tibocha-Bonilla, J.D., Smith, S.R., Coker, J., Allen, A.E., Zengler, K. Constraint-based modeling of diatoms. Metabolism and quantitative biology approaches. In: A. Falciatore and T. Mock (eds) The Molecular Life of Diatoms. Springer Nature Switzerland, p.775-808. 2022.
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Marotz, C., Zuniga, C., Zaramela, L., Knight, R., Zengler, K. Host DNA Depletion in Saliva Samples for Improved Shotgun Metagenomics. In: Adami G.R. (ed) The Oral Microbiome. Methods in Molecular Biology, vol 2327. Humana Press, New York, NY, p.87-92. 2021.
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Tibocha-Bonilla, J.D., Zuniga, C., Godoy-Silva, R.D., Zengler, K. Advances in Metabolic Modeling of Oleaginous Microalgae. In: Prime Archives in Biotechnology. Hyderabad, India: Vide Leaf. 2020.
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Movahedi, N.S., Embree, M., Nagarajan, H., Zengler, K., Chitaz, H. Efficient synergistic single-cell genome assembly. In: Pan, X., Wu, S., Weissman, S.M. (eds) Introduction to Single Cell Omics, Frontiers Media, Lausanne, p.119-127. 2019.
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Zengler, K. Protocols for high throughput isolation and cultivation. In: McGenity, T.J., Timmis, K.N., Nogales, B. (eds) Hydrocarbon and Lipid Microbiology Protocols, Springer-Verlag, Berlin, Heidelberg, New York, p. 27-35. 2014.
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Pappas Jr, G., Barreto, C.C., Ferraz Quirino, B., Krüger, R.H., Zengler, K. Krampis, K. Genome and post-genome technology. In: Rosenberg, E., DeLong, E.F., Thompson, F., Lory, S., Stackebrand, E. (eds) The Prokaryotes, 4th Edition Springer-Verlag, Berlin, Heidelberg, New York, p. 329-344. 2013.
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Zengler, K. To Grow or Not to Grow: Isolation and Cultivation Procedures in the Genomic Age. D.N. Fredricks (ed) The Human Microbiota: How Microbial Communities Affect Health and Disease, John Wiley & Sons, Hoboken, p. 289-302. 2013.
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Zengler, K. Does cultivation still matter? In: Zengler, K. (ed) Accessing Uncultivated Microorganisms: From the Environment to Organisms and Genomes and Back, ASM Press, Washington, DC, p. 3-12. 2008.
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Zengler, K., Paradkar, A., Keller, M. New methods to access microbial diversity for small molecule discovery. In: Zhang, L., Demain, A.L. (eds) Natural Products: Drug Discovery, Therapeutics and Preventive Medicine, Humana Press, Totowa, p. 275-293. 2005.
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Zengler, K. (ed) Accessing Uncultivated Microorganisms: From the Environment to Organisms and Genomes and Back, 2008. ASM Press, Washington, DC.
BOOKS
PREFACE
This book has its origin in a longtime fascination for the diversity of microorganisms and their
sheer endless metabolic capabilities. This fascination was nurtured over the years by multiple
colleagues and friends, which to name all would go far beyond the scope of this preface. However, the person who shaped my view about microorganisms the most and thus contributed to the text being written is Fritz Widdel. As a graduate student in his laboratory at the Max Planck Institute for Marine Microbiology in Bremen, I was not only introduced to principles of thermodynamics and biochemistry but learned to share his affection for isolating and growing microorganisms in the laboratory. As a horticulturist cares for his plants I learned from Fritz how to pamper different microorganisms, pay respect to their needs, and accept their various “temperaments and mood swings.” Observing, understanding, and hopefully predicting these “behaviors” became a driving force for my scientific (ad)ventures. And although nowadays isolation and cultivation are considered by many microbiologists to be old-fashioned, they are still the pillars of microbiology.
Microbially mediated processes are at the center of all global biogeochemical cycles. Solid understanding of processes within a cell, at various levels, is paramount if we are going to apply this knowledge to an understanding of the environment, whether the habitat is the size of a sand grain or the whole ocean floor. Evaluating the microbial diversity and identifying individuals that are responsible for specific processes in the environment are fundamental and challenging tasks in microbial ecology and applied microbiology. It seems appropriate to emphasize the topic of accessing microorganisms and their role in the environment at a time when concomitant advances have been made in various research fields to fulfill these tasks. Researchers address these challenges from different angles, use different methods, and often have different perspectives. It seems that over the course of the last years, however, interdisciplinary research became one of the most successful approaches for ground-breaking discoveries in environmental microbiology. This book highlights various aspects of assessing and accessing microorganisms from the environment and of ways to elucidate basic biological concepts. It spans from critical evaluations on how to determine, define, and measure microbial diversity, including fungi and protists, discussing various cultivation approaches, as well as presenting molecular tool boxes, and reviewing genomic, proteomic, and metagenomic approaches, to single-cell methods, including the development of synthetic cells. I hope this book will inspire researchers and students from various fields to consider all aspects in the exciting challenge of the present microbiological era to understand
and explain the diversity of microorganisms in their environment.
KARSTEN ZENGLER