Multiscale Multiobjective Systems Analysis (MiMoSA): an advanced metabolic modeling framework for complex systems

Gardner, Joseph J.; Hodge, Bri-Mathias S.; Boyle, Nanette R.

doi:10.1038/s41598-019-53188-0

Title: Multiscale Multiobjective Systems Analysis (MiMoSA): an advanced metabolic modeling framework for complex systems

Journal Article · 18 November 2019 · Scientific Reports

DOI: https://doi.org/10.1038/s41598-019-53188-0 · OSTI ID:1619683

Gardner, Joseph J. ^[1];

^[2]; Boyle, Nanette R. ^[1]

Colorado School of Mines, Golden, CO (United States)
Colorado School of Mines, Golden, CO (United States); National Renewable Energy Lab. (NREL), Golden, CO (United States); Univ. of Colorado, Boulder, CO (United States)

In natural environments, cells live in complex communities and experience a high degree of heterogeneity internally and in the environment. Even in 'ideal' laboratory environments, cells can experience a high degree of heterogeneity in their environments. Unfortunately, most of the metabolic modeling approaches that are currently used assume ideal conditions and that each cell is identical, limiting their application to pure cultures in well-mixed vessels. Here we describe our development of Multiscale Multiobjective Systems Analysis (MiMoSA), a metabolic modeling approach that can track individual cells in both space and time, track the diffusion of nutrients and light and the interaction of cells with each other and the environment. As a proof-of concept study, we used MiMoSA to model the growth of Trichodesmium erythraeum, a filamentous diazotrophic cyanobacterium which has cells with two distinct metabolic modes. The use of MiMoSA significantly improves our ability to predictively model metabolic changes and phenotype in more complex cell cultures.

View Journal Article

Cite

Export

Save

Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States); Colorado School of Mines, Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE

Grant/Contract Number:: AC36-08GO28308; SC0019171

OSTI ID:: 1619683

Alternate ID(s):: OSTI ID: 1576586; OSTI ID: 1578262

Report Number(s):: NREL/JA-5D00-75592

Journal Information:: Scientific Reports, Vol. 9, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 6 works

Citation information provided by
Web of Science

References (125)

Heterocyst Development and Localization of Cyanophycin in N2-Fixing Cultures of Anabaena sp. pcc 7120 (Cyanobacteria) Sherman, Debra M.; Tucker, Don; Sherman, Louis A. Journal of Phycology, Vol. 36, Issue 5 https://doi.org/10.1046/j.1529-8817.2000.99132.x	journal	October 2000
d-OptCom: Dynamic Multi-level and Multi-objective Metabolic Modeling of Microbial Communities Zomorrodi, Ali R.; Islam, Mohammad Mazharul; Maranas, Costas D. ACS Synthetic Biology, Vol. 3, Issue 4 https://doi.org/10.1021/sb4001307	journal	November 2013
MAREDAT: towards a world atlas of MARine Ecosystem DATa Buitenhuis, E. T.; Vogt, M.; Moriarty, R. Earth System Science Data, Vol. 5, Issue 2 https://doi.org/10.5194/essd-5-227-2013	journal	January 2013
Effects of growth condition on the structure of glycogen produced in cyanobacterium Synechocystis sp. PCC6803 Yoo, Sang-Ho; Keppel, Catherine; Spalding, Martin International Journal of Biological Macromolecules, Vol. 40, Issue 5 https://doi.org/10.1016/j.ijbiomac.2006.11.009	journal	April 2007
Metabolic Flux Analysis in Plants: From Intelligent Design to Rational Engineering Libourel, Igor G. L.; Shachar-Hill, Yair Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.58.032806.103822	journal	June 2008
In silico approaches to study mass and energy flows in microbial consortia: a syntrophic case study Taffs, Reed; Aston, John E.; Brileya, Kristen BMC Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1186/1752-0509-3-114	journal	January 2009
A multi-paradigm modeling framework for energy systems simulation and analysis Hodge, Bri-Mathias S.; Huang, Shisheng; Siirola, John D. Computers & Chemical Engineering, Vol. 35, Issue 9 https://doi.org/10.1016/j.compchemeng.2011.05.005	journal	September 2011
Integrated Regulatory and Metabolic Networks of the Marine Diatom Phaeodactylum tricornutum Predict the Response to Rising CO ₂ Levels Levering, Jennifer; Dupont, Christopher L.; Allen, Andrew E. mSystems, Vol. 2, Issue 1 https://doi.org/10.1128/mSystems.00142-16	journal	February 2017
Metabolic modeling of a mutualistic microbial community Stolyar, Sergey; Van Dien, Steve; Hillesland, Kristina Linnea Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100131	journal	January 2007
Carbon acquisition by Trichodesmium: the effect of pCO2 and diurnal changes Kranz, Sven A.; Dieter, Sültemeyer; Richter, Klaus-Uwe Limnology and Oceanography, Vol. 54, Issue 2 https://doi.org/10.4319/lo.2009.54.2.0548	journal	March 2009
Metabolic Resource Allocation in Individual Microbes Determines Ecosystem Interactions and Spatial Dynamics Harcombe, William R.; Riehl, William J.; Dukovski, Ilija Cell Reports, Vol. 7, Issue 4 https://doi.org/10.1016/j.celrep.2014.03.070	journal	May 2014
Trichodesmium's strategies to alleviate phosphorus limitation in the future acidified oceans Spungin, D.; Berman-Frank, I.; Levitan, Orly PANGAEA https://doi.org/10.1594/pangaea.833817	dataset	January 2014
A key marine diazotroph in a changing ocean: the interacting effects of temperature, CO2 and light on the growth of Trichodesmium erythraeum IMS101 Boatman, Tobias G.; Lawson, Tracy; Geider, Richard J. PANGAEA https://doi.org/10.1594/pangaea.875042	dataset	January 2017
A Whole-Cell Computational Model Predicts Phenotype from Genotype Karr, Jonathan R.; Sanghvi, Jayodita C.; Macklin, Derek N. Cell, Vol. 150, Issue 2 https://doi.org/10.1016/j.cell.2012.05.044	journal	July 2012
Advances in flux balance analysis Kauffman, Kenneth J.; Prakash, Purusharth; Edwards, Jeremy S. Current Opinion in Biotechnology, Vol. 14, Issue 5 https://doi.org/10.1016/j.copbio.2003.08.001	journal	October 2003
Thermodynamic favorability and pathway yield as evolutionary tradeoffs in biosynthetic pathway choice Du, Bin; Zielinski, Daniel C.; Monk, Jonathan M. Proceedings of the National Academy of Sciences, Vol. 115, Issue 44 https://doi.org/10.1073/pnas.1805367115	journal	October 2018
OptCom: A Multi-Level Optimization Framework for the Metabolic Modeling and Analysis of Microbial Communities Zomorrodi, Ali R.; Maranas, Costas D. PLoS Computational Biology, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pcbi.1002363	journal	February 2012
Metabolic network reconstruction of Chlamydomonas offers insight into light‐driven algal metabolism Chang, Roger L.; Ghamsari, Lila; Manichaikul, Ani Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.52	journal	January 2011
Regulation of nitrogen metabolism in the marine diazotroph Trichodesmium IMS101 under varying temperatures and atmospheric CO2 concentrations: CO2, temperature and Trichodesmium's nitrogen metabolism Levitan, Orly; Brown, Christopher M.; Sudhaus, Stefanie Environmental Microbiology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1462-2920.2010.02195.x	journal	March 2010
Nitrogen fixation and growth rates of Trichodesmium IMS-101 as a function of light intensity Breitbarth, E.; Wohlers, J.; Kläs, J. Marine Ecology Progress Series, Vol. 359 https://doi.org/10.3354/meps07241	journal	May 2008
MAREDAT: towards a world atlas of MARine Ecosystem DATa Buitenhuis, Erik T.; Vogt, Meike; Moriarty, Róisín ETH Zurich https://doi.org/10.3929/ethz-b-000073329	text	January 2013
Genome-Scale Reconstruction of the Saccharomyces cerevisiae Metabolic Network Forster, J. Genome Research, Vol. 13, Issue 2 https://doi.org/10.1101/gr.234503	journal	February 2003
The physiological cost of diazotrophy for Trichodesmium erythraeum IMS101 Boatman, Tobias G.; Davey, Phillip A.; Lawson, Tracy PLOS ONE, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pone.0195638	journal	April 2018
Additional file 6: of The use of genome-scale metabolic network reconstruction to predict fluxes and equilibrium composition of N-fixing versus C-fixing cells in a diazotrophic cyanobacterium, Trichodesmium erythraeum Gardner, Joseph; Boyle, Nanette Figshare https://doi.org/10.6084/m9.figshare.c.3670009_d8.v1	dataset	January 2017
Systems metabolic engineering: Genome-scale models and beyond Blazeck, John; Alper, Hal Biotechnology Journal, Vol. 5, Issue 7 https://doi.org/10.1002/biot.200900247	journal	February 2010
Electron transport kinetics in the diazotrophic cyanobacterium Trichodesmium spp. grown across a range of light levels Cai, Xiaoni; Gao, Kunshan; Fu, Feixue Photosynthesis Research, Vol. 124, Issue 1 https://doi.org/10.1007/s11120-015-0081-5	journal	January 2015
The estimation of carbohydrates in plant extracts by anthrone Yemm, E. W.; Willis, A. J. Biochemical Journal, Vol. 57, Issue 3 https://doi.org/10.1042/bj0570508	journal	July 1954
Modification of the Sakaguchi reaction: Spectrophotometric determination of arginine in proteins without previous hydrolysis Messineo, Luigi Archives of Biochemistry and Biophysics, Vol. 117, Issue 3 https://doi.org/10.1016/0003-9861(66)90094-4	journal	December 1966
Compartmentalized cyanophycin metabolism in the diazotrophic filaments of a heterocyst-forming cyanobacterium Burnat, Mireia; Herrero, Antonia; Flores, Enrique Proceedings of the National Academy of Sciences, Vol. 111, Issue 10 https://doi.org/10.1073/pnas.1318564111	journal	February 2014
Inorganic carbon and pH dependency of photosynthetic rates in Trichodesmium Boatman, Tobias G.; Mangan, Niall M.; Lawson, Tracy Journal of Experimental Botany, Vol. 69, Issue 15 https://doi.org/10.1093/jxb/ery141	journal	April 2018
Exploring Multi-Paradigm Modeling Techniques Hardebolle, Cécile; Boulanger, Frédéric SIMULATION, Vol. 85, Issue 11-12 https://doi.org/10.1177/0037549709105240	journal	July 2009
Cellular inorganic carbon fluxes in Trichodesmium: a combined approach using measurements and modelling Eichner, Meri; Thoms, Silke; Kranz, Sven A. Journal of Experimental Botany, Vol. 66, Issue 3 https://doi.org/10.1093/jxb/eru427	journal	November 2014
CO ₂ control of Trichodesmium N ₂ fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry Hutchins, D. A.; Fu, F. -X.; Zhang, Y. Limnology and Oceanography, Vol. 52, Issue 4 https://doi.org/10.4319/lo.2007.52.4.1293	journal	July 2007
Cyanophycin Granules from the Blue-Green Alga Anabaena cylindrica: A Reserve Material Consisting of Copolymers of Aspartic Acid and Arginine Simon, R. D. Proceedings of the National Academy of Sciences, Vol. 68, Issue 2 https://doi.org/10.1073/pnas.68.2.265	journal	February 1971
Flux Balance Analysis of Cyanobacterial Metabolism: The Metabolic Network of Synechocystis sp. PCC 6803 Knoop, Henning; Gründel, Marianne; Zilliges, Yvonne PLoS Computational Biology, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pcbi.1003081	journal	June 2013
Global transcriptional regulatory network for Escherichia coli robustly connects gene expression to transcription factor activities Fang, Xin; Sastry, Anand; Mih, Nathan Proceedings of the National Academy of Sciences, Vol. 114, Issue 38 https://doi.org/10.1073/pnas.1702581114	journal	September 2017
Elucidation of complexity and prediction of interactions in microbial communities Zuñiga, Cristal; Zaramela, Livia; Zengler, Karsten Microbial Biotechnology, Vol. 10, Issue 6 https://doi.org/10.1111/1751-7915.12855	journal	August 2017
The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains Breuer, Guido; Lamers, Packo P.; Martens, Dirk E. Bioresource Technology, Vol. 124 https://doi.org/10.1016/j.biortech.2012.08.003	journal	November 2012
Global transcriptional regulatory network for Escherichia coli robustly connects gene expression to transcription factor activities Fang, Xin; Sastry, Anand; Mih, Nathan Proceedings of the National Academy of Sciences, Vol. 114, Issue 38 https://doi.org/10.1073/pnas.1702581114	journal	September 2017
Systems-Level Analysis of Nitrogen Starvation-Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant Blaby, I. K.; Glaesener, A. G.; Mettler, T. The Plant Cell, Vol. 25, Issue 11 https://doi.org/10.1105/tpc.113.117580	journal	November 2013
Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria Berman-Frank, Ilana; Lundgren, Pernilla; Falkowski, Paul Research in Microbiology, Vol. 154, Issue 3 https://doi.org/10.1016/S0923-2508(03)00029-9	journal	April 2003
Growth and Nitrogen Fixation of the Diazotrophic Filamentous Nonheterocystous Cyanobacterium Trichodesmium sp. ims 101 in Defined Media: Evidence for a Circadian Rhythm1 Chen, Yi-Bu; Zehr, Jonathan P.; Mellon, Mark Journal of Phycology, Vol. 32, Issue 6 https://doi.org/10.1111/j.0022-3646.1996.00916.x	journal	December 1996
Modeling Growth Kinetics, Interspecies Cell Fusion, and Metabolism of a Clostridium acetobutylicum/Clostridium ljungdahlii Syntrophic Coculture Foster, Charles; Charubin, Kamil; Papoutsakis, Eleftherios T. mSystems, Vol. 6, Issue 1 https://doi.org/10.1128/msystems.01325-20	journal	February 2021
Electron transport kinetics in the diazotrophic cyanobacterium Trichodesmium spp. grown across a range of light levels Cai, Xiaoni; Gao, Kunshan; Fu, Feixue Photosynthesis Research, Vol. 124, Issue 1 https://doi.org/10.1007/s11120-015-0081-5	journal	January 2015
Effects of ectomycorrhizal fungi (Suillus variegatus) on the growth, hydraulic function, and non-structural carbohydrates of Pinus tabulaeformis under drought stress Wang, Jiaxing; Zhang, Haoqiang; Gao, Jing BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-021-02945-3	journal	April 2021
Ecological modelling in a sea of variable stoichiometry: Dysfunctionality and the legacy of Redfield and Monod Flynn, Kevin J. Progress in Oceanography, Vol. 84, Issue 1-2 https://doi.org/10.1016/j.pocean.2009.09.006	journal	January 2010
Modification of the Sakaguchi reaction: Spectrophotometric determination of arginine in proteins without previous hydrolysis Messineo, Luigi Archives of Biochemistry and Biophysics, Vol. 117, Issue 3 https://doi.org/10.1016/0003-9861(66)90094-4	journal	December 1966
A Key Marine Diazotroph in a Changing Ocean: The Interacting Effects of Temperature, CO2 and Light on the Growth of Trichodesmium erythraeum IMS101 Boatman, Tobias G.; Lawson, Tracy; Geider, Richard J. PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0168796	journal	January 2017
Additional file 6: of The use of genome-scale metabolic network reconstruction to predict fluxes and equilibrium composition of N-fixing versus C-fixing cells in a diazotrophic cyanobacterium, Trichodesmium erythraeum Gardner, Joseph; Boyle, Nanette Figshare https://doi.org/10.6084/m9.figshare.c.3670009_d8	dataset	January 2017
Modeling formalisms in Systems Biology Machado, Daniel; Costa, Rafael S.; Rocha, Miguel AMB Express, Vol. 1, Issue 1 https://doi.org/10.1186/2191-0855-1-45	journal	January 2011
Computer Automated Multi-Paradigm Modeling: An Introduction Mosterman, Pieter J.; Vangheluwe, Hans SIMULATION, Vol. 80, Issue 9 https://doi.org/10.1177/0037549704050532	journal	September 2004
Database of diazotrophs in global ocean: abundance, biomass and nitrogen fixation rates Luo, Y. -W.; Doney, S. C.; Anderson, L. A. Earth System Science Data, Vol. 4, Issue 1 https://doi.org/10.5194/essd-4-47-2012	journal	January 2012
Dynamic Flux Balance Analysis of Diauxic Growth in Escherichia coli Mahadevan, Radhakrishnan; Edwards, Jeremy S.; Doyle, Francis J. Biophysical Journal, Vol. 83, Issue 3 https://doi.org/10.1016/S0006-3495(02)73903-9	journal	September 2002
Applications of genome‐scale metabolic reconstructions Oberhardt, Matthew A.; Palsson, Bernhard Ø; Papin, Jason A. Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.77	journal	January 2009
Evolution of species interactions determines microbial community productivity in new environments Fiegna, Francesca; Moreno-Letelier, Alejandra; Bell, Thomas The ISME Journal, Vol. 9, Issue 5 https://doi.org/10.1038/ismej.2014.215	journal	November 2014
Characterization and modelling of interspecies electron transfer mechanisms and microbial community dynamics of a syntrophic association Nagarajan, Harish; Embree, Mallory; Rotaru, Amelia-Elena Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3809	journal	November 2013
Metabolic modeling of a mutualistic microbial community Stolyar, Sergey; Van Dien, Steve; Hillesland, Kristina Linnea Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100131	journal	January 2007
Multi-Paradigm Modeling of the Effects of PHEV Adoption on Electric Utility Usage Levels and Emissions Hodge, Bri-Mathias; Shukla, Aviral; Huang, Shisheng Industrial & Engineering Chemistry Research, Vol. 50, Issue 9 https://doi.org/10.1021/ie101837w	journal	May 2011
Systems-level characterization of a host-microbe metabolic symbiosis in the mammalian gut Heinken, Almut; Sahoo, Swagatika; Fleming, Ronan M. T. Gut Microbes, Vol. 4, Issue 1 https://doi.org/10.4161/gmic.22370	journal	January 2013
The primary transcriptome of the marine diazotroph Trichodesmium erythraeum IMS101 Pfreundt, Ulrike; Kopf, Matthias; Belkin, Natalia Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06187	journal	August 2014
Metabolic modeling of microbial strains in silico Covert, Markus W.; Schilling, Christophe H.; Famili, Iman Trends in Biochemical Sciences, Vol. 26, Issue 3 https://doi.org/10.1016/S0968-0004(00)01754-0	journal	March 2001
Metabolic Flux Analysis in Plants: From Intelligent Design to Rational Engineering Libourel, Igor G. L.; Shachar-Hill, Yair Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.58.032806.103822	journal	June 2008
The effects of alternate optimal solutions in constraint-based genome-scale metabolic models Mahadevan, R.; Schilling, C. H. Metabolic Engineering, Vol. 5, Issue 4 https://doi.org/10.1016/j.ymben.2003.09.002	journal	October 2003
Advances in flux balance analysis Kauffman, Kenneth J.; Prakash, Purusharth; Edwards, Jeremy S. Current Opinion in Biotechnology, Vol. 14, Issue 5 https://doi.org/10.1016/j.copbio.2003.08.001	journal	October 2003
T richodesmium 's strategies to alleviate phosphorus limitation in the future acidified oceans Spungin, Dina; Berman-Frank, Ilana; Levitan, Orly Environmental Microbiology, Vol. 16, Issue 6 https://doi.org/10.1111/1462-2920.12424	journal	March 2014
Evolution of species interactions determines microbial community productivity in new environments Francesca, Fiegna,; Alejandra, Moreno-Letelier,; Thomas, Bell, ETH Zurich https://doi.org/10.3929/ethz-b-000094271	text	January 2015
A multi-paradigm modeling framework for energy systems simulation and analysis Hodge, Bri-Mathias S.; Huang, Shisheng; Siirola, John D. Computers & Chemical Engineering, Vol. 35, Issue 9 https://doi.org/10.1016/j.compchemeng.2011.05.005	journal	September 2011
The use of genome-scale metabolic network reconstruction to predict fluxes and equilibrium composition of N-fixing versus C-fixing cells in a diazotrophic cyanobacterium, Trichodesmium erythraeum Gardner, Joseph J.; Boyle, Nanette R. BMC Systems Biology, Vol. 11, Issue 1 https://doi.org/10.1186/s12918-016-0383-z	journal	January 2017
Three Acyltransferases and Nitrogen-responsive Regulator Are Implicated in Nitrogen Starvation-induced Triacylglycerol Accumulation in Chlamydomonas Boyle, Nanette R.; Page, Mark Dudley; Liu, Bensheng Journal of Biological Chemistry, Vol. 287, Issue 19 https://doi.org/10.1074/jbc.M111.334052	journal	March 2012
Segregation of Nitrogen Fixation and Oxygenic Photosynthesis in the Marine Cyanobacterium Trichodesmium Berman-Frank, I. Science, Vol. 294, Issue 5546 https://doi.org/10.1126/science.1064082	journal	November 2001
N ₂ fixation in free‐floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments Eichner, Meri; Thoms, Silke; Rost, Björn New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15621	journal	December 2018
The Response of Diatom Central Carbon Metabolism to Nitrogen Starvation Is Different from That of Green Algae and Higher Plants Hockin, Nicola Louise; Mock, Thomas; Mulholland, Francis Plant Physiology, Vol. 158, Issue 1 https://doi.org/10.1104/pp.111.184333	journal	November 2011
CO2 modulation of the rates of photosynthesis and light-dependent O2 consumption in Trichodesmium Boatman, Tobias G.; Davey, Phillip A.; Lawson, Tracy Journal of Experimental Botany, Vol. 70, Issue 2 https://doi.org/10.1093/jxb/ery368	journal	October 2018
Heterocyst Development and Localization of Cyanophycin in N2-Fixing Cultures of Anabaena sp. pcc 7120 (Cyanobacteria) Sherman, Debra M.; Tucker, Don; Sherman, Louis A. Journal of Phycology, Vol. 36, Issue 5 https://doi.org/10.1046/j.1529-8817.2000.99132.x	journal	October 2000
Spatial and temporal distribution of Trichodesmium blooms in the world's oceans : TRICHODESMIUM BLOOMS Westberry, Toby K.; Siegel, David A. Global Biogeochemical Cycles, Vol. 20, Issue 4 https://doi.org/10.1029/2005GB002673	journal	December 2006
Applications of genome‐scale metabolic reconstructions Oberhardt, Matthew A.; Palsson, Bernhard Ø; Papin, Jason A. Molecular Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1038/msb.2009.77	journal	January 2009
In silico approaches to study mass and energy flows in microbial consortia: a syntrophic case study Taffs, Reed; Aston, John E.; Brileya, Kristen BMC Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1186/1752-0509-3-114	journal	January 2009
The estimation of carbohydrates in plant extracts by anthrone Yemm, E. W.; Willis, A. J. Biochemical Journal, Vol. 57, Issue 3 https://doi.org/10.1042/bj0570508	journal	July 1954
A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii: A revised mineral nutrient supplement for Chlamydomonas Kropat, Janette; Hong-Hermesdorf, Anne; Casero, David The Plant Journal, Vol. 66, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04537.x	journal	March 2011
OptCom: A Multi-Level Optimization Framework for the Metabolic Modeling and Analysis of Microbial Communities Zomorrodi, Ali R.; Maranas, Costas D. PLoS Computational Biology, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pcbi.1002363	journal	February 2012
The ultrastructure of the marine blue green alga, Trichodesmium erythraeum, with special reference to the cell wall, gas vacuoles, and cylindrical bodies Baalen, Chase; Brown, R. Malcolm Archiv f�r Mikrobiologie, Vol. 69, Issue 1 https://doi.org/10.1007/BF00408566	journal	January 1969
Systematic evaluation of objective functions for predicting intracellular fluxes in Escherichia coli Schuetz, Robert; Kuepfer, Lars; Sauer, Uwe ETH Zurich https://doi.org/10.3929/ethz-b-000004128	text	January 2007
Predicting Dynamic Metabolic Demands in the Photosynthetic Eukaryote Chlorella vulgaris Zuñiga, Cristal; Levering, Jennifer; Antoniewicz, Maciek R. Plant Physiology, Vol. 176, Issue 1 https://doi.org/10.1104/pp.17.00605	journal	September 2017
Temporal Variability of Trichodesmium spp. and Diatom-Diazotroph Assemblages in the North Pacific Subtropical Gyre White, Angelicque E.; Watkins-Brandt, Katie S.; Church, Matthew J. Frontiers in Marine Science, Vol. 5 https://doi.org/10.3389/fmars.2018.00027	journal	February 2018
Light, temperature and nitrogen starvation effects on the total lipid and fatty acid content and composition ofSpirulina platensis UTEX 1928 Tedesco, Mark A.; Duerr, Eirik O. Journal of Applied Phycology, Vol. 1, Issue 3 https://doi.org/10.1007/bf00003646	journal	November 1989
Comparative proteomic profiles of the marine cyanobacterium Trichodesmium erythraeum IMS101 under different nitrogen regimes Sandh, Gustaf; Ran, Liang; Xu, Linghua PROTEOMICS, Vol. 11, Issue 3 https://doi.org/10.1002/pmic.201000382	journal	January 2011
Enhancing sesquiterpene production in Saccharomyces cerevisiae through in silico driven metabolic engineering Asadollahi, Mohammad A.; Maury, Jérôme; Patil, Kiran Raosaheb Metabolic Engineering, Vol. 11, Issue 6, p. 328-334 https://doi.org/10.1016/j.ymben.2009.07.001	journal	November 2009
The effects of alternate optimal solutions in constraint-based genome-scale metabolic models Mahadevan, R.; Schilling, C. H. Metabolic Engineering, Vol. 5, Issue 4 https://doi.org/10.1016/j.ymben.2003.09.002	journal	October 2003
A Whole-Cell Computational Model Predicts Phenotype from Genotype Karr, Jonathan R.; Sanghvi, Jayodita C.; Macklin, Derek N. Cell, Vol. 150, Issue 2 https://doi.org/10.1016/j.cell.2012.05.044	journal	July 2012
The determination of ammonia in seawater Liddicoat, M. I.; Tibhitts, Susan; Butler, E. I. Limnology and Oceanography, Vol. 20, Issue 1 https://doi.org/10.4319/lo.1975.20.1.0131	journal	January 1975
Agent-based simulation of reactions in the crowded and structured intracellular environment: influence of mobility and location of the reactants T., Klann, Michael; Alexei, Lapin,; Matthias, Reuss, ETH Zurich https://doi.org/10.3929/ethz-b-000037890	text	January 2011
Identifying control mechanisms of granuloma formation during M. tuberculosis infection using an agent-based model Segovia-Juarez, Jose L.; Ganguli, Suman; Kirschner, Denise Journal of Theoretical Biology, Vol. 231, Issue 3 https://doi.org/10.1016/j.jtbi.2004.06.031	journal	December 2004
Systematic evaluation of objective functions for predicting intracellular fluxes in Escherichia coli Schuetz, Robert; Kuepfer, Lars; Sauer, Uwe Molecular Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1038/msb4100162	journal	January 2007
The design of long-term effective uranium bioremediation strategy using a community metabolic model Zhuang, K.; Ma, E.; Lovley, Derek R. Biotechnology and Bioengineering, Vol. 109, Issue 10 https://doi.org/10.1002/bit.24528	journal	April 2012
Characterization and modelling of interspecies electron transfer mechanisms and microbial community dynamics of a syntrophic association Nagarajan, Harish; Embree, Mallory; Rotaru, Amelia-Elena Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3809	journal	November 2013
Parallel agent-based simulation with Repast for High Performance Computing Collier, Nicholson; North, Michael SIMULATION, Vol. 89, Issue 10 https://doi.org/10.1177/0037549712462620	journal	November 2012
Cellular inorganic carbon fluxes in Trichodesmium: a combined approach using measurements and modelling Eichner, Meri; Thoms, Silke; Kranz, Sven A. Journal of Experimental Botany, Vol. 66, Issue 3 https://doi.org/10.1093/jxb/eru427	journal	November 2014
CO ₂ control of Trichodesmium N ₂ fixation, photosynthesis, growth rates, and elemental ratios: Implications for past, present, and future ocean biogeochemistry Hutchins, D. A.; Fu, F. -X.; Zhang, Y. Limnology and Oceanography, Vol. 52, Issue 4 https://doi.org/10.4319/lo.2007.52.4.1293	journal	July 2007
Systems-Level Analysis of Nitrogen Starvation-Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant Blaby, I. K.; Glaesener, A. G.; Mettler, T. The Plant Cell, Vol. 25, Issue 11 https://doi.org/10.1105/tpc.113.117580	journal	November 2013
Metabolic analyses elucidate non-trivial gene targets for amplifying dihydroartemisinic acid production in yeast Misra, Ashish; Conway, Matthew F.; Johnnie, Joseph Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00200	journal	January 2013
Flux Balance Analysis of Cyanobacterial Metabolism: The Metabolic Network of Synechocystis sp. PCC 6803 Knoop, Henning; Gründel, Marianne; Zilliges, Yvonne PLoS Computational Biology, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pcbi.1003081	journal	June 2013
Multi-Paradigm Modeling of the Effects of PHEV Adoption on Electric Utility Usage Levels and Emissions Hodge, Bri-Mathias; Shukla, Aviral; Huang, Shisheng Industrial & Engineering Chemistry Research, Vol. 50, Issue 9 https://doi.org/10.1021/ie101837w	journal	May 2011
Identifying control mechanisms of granuloma formation during M. tuberculosis infection using an agent-based model Segovia-Juarez, Jose L.; Ganguli, Suman; Kirschner, Denise Journal of Theoretical Biology, Vol. 231, Issue 3 https://doi.org/10.1016/j.jtbi.2004.06.031	journal	December 2004
Systems-level characterization of a host-microbe metabolic symbiosis in the mammalian gut Heinken, Almut; Sahoo, Swagatika; Fleming, Ronan M. T. Gut Microbes, Vol. 4, Issue 1 https://doi.org/10.4161/gmic.22370	journal	January 2013
Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii Boyle, Nanette R.; Morgan, John A. BMC Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1186/1752-0509-3-4	journal	January 2009
Genome-Scale Reconstruction of the Saccharomyces cerevisiae Metabolic Network Forster, J. Genome Research, Vol. 13, Issue 2 https://doi.org/10.1101/gr.234503	journal	February 2003
Modeling formalisms in Systems Biology Machado, Daniel; Costa, Rafael S.; Rocha, Miguel AMB Express, Vol. 1, Issue 1 https://doi.org/10.1186/2191-0855-1-45	journal	January 2011
Harnessing the landscape of microbial culture media to predict new organism–media pairings Oberhardt, Matthew A.; Zarecki, Raphy; Gronow, Sabine Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9493	journal	October 2015
The primary transcriptome of the marine diazotroph Trichodesmium erythraeum IMS101 Pfreundt, Ulrike; Kopf, Matthias; Belkin, Natalia Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06187	journal	August 2014
A Key Marine Diazotroph in a Changing Ocean: The Interacting Effects of Temperature, CO2 and Light on the Growth of Trichodesmium erythraeum IMS101 Boatman, Tobias G.; Lawson, Tracy; Geider, Richard J. PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0168796	journal	January 2017
The physiological cost of diazotrophy for Trichodesmium erythraeum IMS101 Boatman, Tobias G.; Davey, Phillip A.; Lawson, Tracy PLOS ONE, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pone.0195638	journal	April 2018
Parallel agent-based simulation with Repast for High Performance Computing Collier, Nicholson; North, Michael SIMULATION, Vol. 89, Issue 10 https://doi.org/10.1177/0037549712462620	journal	November 2012
Computer Automated Multi-Paradigm Modeling: An Introduction Mosterman, Pieter J.; Vangheluwe, Hans SIMULATION, Vol. 80, Issue 9 https://doi.org/10.1177/0037549704050532	journal	September 2004
Release of Dissolved Organic Nitrogen by Marine Diazotrophic Cyanobacteria, Trichodesmium spp. † Glibert, Patricia M.; Bronk, Deborah A. Applied and Environmental Microbiology, Vol. 60, Issue 11 https://doi.org/10.1128/aem.60.11.3996-4000.1994	journal	January 1994
Carbon acquisition by Trichodesmium: the effect of pCO2 and diurnal changes Kranz, Sven A.; Dieter, Sültemeyer; Richter, Klaus-Uwe Limnology and Oceanography, Vol. 54, Issue 2 https://doi.org/10.4319/lo.2009.54.2.0548	journal	March 2009
Metabolic Resource Allocation in Individual Microbes Determines Ecosystem Interactions and Spatial Dynamics Harcombe, William R.; Riehl, William J.; Dukovski, Ilija Cell Reports, Vol. 7, Issue 4 https://doi.org/10.1016/j.celrep.2014.03.070	journal	May 2014
The Response of Diatom Central Carbon Metabolism to Nitrogen Starvation Is Different from That of Green Algae and Higher Plants Hockin, Nicola Louise; Mock, Thomas; Mulholland, Francis Plant Physiology, Vol. 158, Issue 1 https://doi.org/10.1104/pp.111.184333	journal	November 2011
Growth and Nitrogen Fixation of the Diazotrophic Filamentous Nonheterocystous Cyanobacterium Trichodesmium sp. ims 101 in Defined Media: Evidence for a Circadian Rhythm1 Chen, Yi-Bu; Zehr, Jonathan P.; Mellon, Mark Journal of Phycology, Vol. 32, Issue 6 https://doi.org/10.1111/j.0022-3646.1996.00916.x	journal	December 1996
Agent-based simulation of reactions in the crowded and structured intracellular environment: influence of mobility and location of the reactants T., Klann, Michael; Alexei, Lapin,; Matthias, Reuss, ETH Zurich https://doi.org/10.3929/ethz-b-000037890	text	January 2011
What is flux balance analysis? Orth, Jeffrey D.; Thiele, Ines; Palsson, Bernhard Ø Nature Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1038/nbt.1614	journal	March 2010
CO2 modulation of the rates of photosynthesis and light-dependent O2 consumption in Trichodesmium Boatman, Tobias G.; Davey, Phillip A.; Lawson, Tracy Journal of Experimental Botany, Vol. 70, Issue 2 https://doi.org/10.1093/jxb/ery368	journal	October 2018
Elucidation of complexity and prediction of interactions in microbial communities Zuñiga, Cristal; Zaramela, Livia; Zengler, Karsten Microbial Biotechnology, Vol. 10, Issue 6 https://doi.org/10.1111/1751-7915.12855	journal	August 2017
The Tricarboxylic Acid Cycle in Cyanobacteria Zhang, S.; Bryant, D. A. Science, Vol. 334, Issue 6062 https://doi.org/10.1126/science.1210858	journal	December 2011
Agent-based simulation of reactions in the crowded and structured intracellular environment: Influence of mobility and location of the reactants Klann, Michael T.; Lapin, Alexei; Reuss, Matthias BMC Systems Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1752-0509-5-71	journal	January 2011
Release of Dissolved Organic Nitrogen by Marine Diazotrophic Cyanobacteria, Trichodesmium spp. † Glibert, Patricia M.; Bronk, Deborah A. Applied and Environmental Microbiology, Vol. 60, Issue 11 https://doi.org/10.1128/aem.60.11.3996-4000.1994	journal	January 1994

Similar Records

Investigating the Unique Ability of Trichodesmium To Fix Carbon and Nitrogen Simultaneously Using MiMoSA

Journal Article · 2023 · mSystems · OSTI ID:1924018

Gardner, Joseph J.; Hodge, Bri-Mathias S.; Boyle, Nanette R.

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Journal Article · 2015 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1208769

Walworth, Nathan; Pfreundt, Ulrike; Nelson, William C.; +12 more

Taxonomic distribution of metabolic functions in bacteria associated with Trichodesmium consortia

Journal Article · 2023 · mSystems · OSTI ID:2367185

Koedooder, Coco; Zhang, Futing; Wang, Siyuan; +10 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
biochemistry
computational models
metabolic engineering
microbial ecology
60 APPLIED LIFE SCIENCES
59 BASIC BIOLOGICAL SCIENCES
09 BIOMASS FUELS
metabolic flux
agent based modeling
consortia
nitrogen fixation

Title: Multiscale Multiobjective Systems Analysis (MiMoSA): an advanced metabolic modeling framework for complex systems

Citation Formats

References (125)

Similar Records

Related Subjects