Probabilistic Modeling of Microbial Metabolic Networks for Integrating Partial Quantitative Knowledge Within the Nitrogen Cycle

Eveillard, Damien; Bouskill, Nicholas J.; Vintache, Damien; Gras, Julien; Ward, Bess B.; Bourdon, Jérémie

doi:10.3389/fmicb.2018.03298

Title: Probabilistic Modeling of Microbial Metabolic Networks for Integrating Partial Quantitative Knowledge Within the Nitrogen Cycle

Journal Article · 28 January 2019 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2018.03298 · OSTI ID:1561879

Eveillard, Damien ^[1]; Bouskill, Nicholas J. ^[2]; Vintache, Damien ^[1]; Gras, Julien ^[3]; Ward, Bess B. ^[4]; Bourdon, Jérémie ^[3]

Univ. de Nantes, Nantes (France). Centrale Nantes; Research Federation (FR2022) Tara Oceans Global Ocean System Ecology & Evolution (GO-SEE), Paris (France)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. de Nantes, Nantes (France). Centrale Nantes
Princeton Univ., NJ (United States)

Understanding the interactions between microbial communities and their environment sufficiently to predict diversity on the basis of physicochemical parameters is a fundamental pursuit of microbial ecology that still eludes us. However, modeling microbial communities is problematic, because (i) communities are complex, (ii) most descriptions are qualitative, and (iii) quantitative understanding of the way communities interact with their surroundings remains incomplete. One approach to overcoming such complications is the integration of partial qualitative and quantitative descriptions into more complex networks. Here we outline the development of a probabilistic framework, based on Event Transition Graph (ETG) theory, to predict microbial community structure across observed chemical data. Using reverse engineering, we derive probabilities from the ETG that accurately represent observations from experiments and predict putative constraints on communities within dynamic environments. These predictions can feedback into the future development of field experiments by emphasizing the most important functional reactions, and associated microbial strains, required to characterize microbial ecosystems.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1561879

Journal Information:: Frontiers in Microbiology, Vol. 9, Issue JAN; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

Microbial interactions: from networks to models Faust, Karoline; Raes, Jeroen Nature Reviews Microbiology, Vol. 10, Issue 8 https://doi.org/10.1038/nrmicro2832	journal	July 2012
Ecosystems biology of microbial metabolism Klitgord, Niels; Segrè, Daniel Current Opinion in Biotechnology, Vol. 22, Issue 4 https://doi.org/10.1016/j.copbio.2011.04.018	journal	August 2011
Computational meta'omics for microbial community studies Segata, Nicola; Boernigen, Daniela; Tickle, Timothy L. Molecular Systems Biology, Vol. 9, Issue 1 https://doi.org/10.1038/msb.2013.22	journal	January 2013
Toward molecular trait‐based ecology through integration of biogeochemical, geographical and metagenomic data Raes, Jeroen; Letunic, Ivica; Yamada, Takuji Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.6	journal	January 2011
Integrating Quantitative Knowledge into a Qualitative Gene Regulatory Network Bourdon, Jérémie; Eveillard, Damien; Siegel, Anne PLoS Computational Biology, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pcbi.1002157	journal	September 2011
Ecological Systems as Complex Systems: Challenges for an Emerging Science Anand, Madhur; Gonzalez, Andrew; Guichard, Frédéric Diversity, Vol. 2, Issue 3 https://doi.org/10.3390/d2030395	journal	March 2010
Analyzing Tropical Forest Tree Species Abundance Distributions Using a Nonneutral Model and through Approximate Bayesian Inference Jabot, Franck; Chave, Jérôme The American Naturalist, Vol. 178, Issue 2 https://doi.org/10.1086/660829	journal	August 2011
A Logic for Checking the Probabilistic Steady-State Properties of Reaction Networks Picard, Vincent; Siegel, Anne; Bourdon, Jérémie Journal of Computational Biology, Vol. 24, Issue 8 https://doi.org/10.1089/cmb.2017.0099	journal	August 2017
Ocean biogeochemistry modeled with emergent trait-based genomics Coles, V. J.; Stukel, M. R.; Brooks, M. T. Science, Vol. 358, Issue 6367 https://doi.org/10.1126/science.aan5712	journal	November 2017
Putative bacterial interactions from metagenomic knowledge with an integrative systems ecology approach Bordron, Philippe; Latorre, Mauricio; Cortés, Maria-Paz MicrobiologyOpen, Vol. 5, Issue 1 https://doi.org/10.1002/mbo3.315	journal	December 2015
Probabilistic Boolean networks: a rule-based uncertainty model for gene regulatory networks Shmulevich, I.; Dougherty, E. R.; Kim, S. Bioinformatics, Vol. 18, Issue 2 https://doi.org/10.1093/bioinformatics/18.2.261	journal	February 2002
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Analysis of membrane proteins in metagenomics: Networks of correlated environmental features and protein families Patel, P. V.; Gianoulis, T. A.; Bjornson, R. D. Genome Research, Vol. 20, Issue 7 https://doi.org/10.1101/gr.102814.109	journal	April 2010
Metabolic Network Modeling of Microbial Interactions in Natural and Engineered Environmental Systems Perez-Garcia, Octavio; Lear, Gavin; Singhal, Naresh Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00673	journal	May 2016
Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer Jewell, Talia N. M.; Karaoz, Ulas; Brodie, Eoin L. The ISME Journal, Vol. 10, Issue 9 https://doi.org/10.1038/ismej.2016.25	journal	March 2016
Future paths for integer programming and links to artificial intelligence Glover, Fred Computers & Operations Research, Vol. 13, Issue 5 https://doi.org/10.1016/0305-0548(86)90048-1	journal	January 1986
Molecular eco-systems biology: towards an understanding of community function Raes, Jeroen; Bork, Peer Nature Reviews Microbiology, Vol. 6, Issue 9 https://doi.org/10.1038/nrmicro1935	journal	June 2008
A multi-objective constraint-based approach for modeling genome-scale microbial ecosystems Budinich, Marko; Bourdon, Jérémie; Larhlimi, Abdelhalim PLOS ONE, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pone.0171744	journal	February 2017
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
Using Bayesian Networks to Analyze Expression Data Friedman, Nir; Linial, Michal; Nachman, Iftach Journal of Computational Biology, Vol. 7, Issue 3-4 https://doi.org/10.1089/106652700750050961	journal	August 2000
Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years Cram, Jacob A.; Chow, Cheryl-Emiliane T.; Sachdeva, Rohan The ISME Journal, Vol. 9, Issue 3 https://doi.org/10.1038/ismej.2014.153	journal	September 2014
Marine microbial community dynamics and their ecological interpretation Fuhrman, Jed A.; Cram, Jacob A.; Needham, David M. Nature Reviews Microbiology, Vol. 13, Issue 3 https://doi.org/10.1038/nrmicro3417	journal	February 2015
Where Next for Microbiome Research? Waldor, Matthew K.; Tyson, Gene; Borenstein, Elhanan PLOS Biology, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pbio.1002050	journal	January 2015
Parameter and uncertainty estimation for process-oriented population and distribution models: data, statistics and the niche Marion, Glenn; McInerny, Greg J.; Pagel, Jörn Journal of Biogeography, Vol. 39, Issue 12 https://doi.org/10.1111/j.1365-2699.2012.02772.x	journal	September 2012
Ammonia-oxidizing bacterial community composition in estuarine and oceanic environments assessed using a functional gene microarray Ward, Bess B.; Eveillard, Damien; Kirshtein, Julie D. Environmental Microbiology, Vol. 9, Issue 10 https://doi.org/10.1111/j.1462-2920.2007.01371.x	journal	October 2007
Plankton networks driving carbon export in the oligotrophic ocean Guidi, Lionel; Chaffron, Samuel; Bittner, Lucie Nature, Vol. 532, Issue 7600 https://doi.org/10.1038/nature16942	journal	February 2016
Multivariate Normal Approximation for the Stochastic Simulation Algorithm: Limit Theorem and Applications Picard, Vincent; Siegel, Anne; Bourdon, Jérémie Electronic Notes in Theoretical Computer Science, Vol. 316 https://doi.org/10.1016/j.entcs.2015.06.011	journal	September 2015
Seasonal and annual reoccurrence in betaproteobacterial ammonia-oxidizing bacterial population structure: Seasonally reoccurring AOB communities Bouskill, Nicholas J.; Eveillard, Damien; O'Mullan, Gregory Environmental Microbiology, Vol. 13, Issue 4 https://doi.org/10.1111/j.1462-2920.2010.02362.x	journal	November 2010
Annually reoccurring bacterial communities are predictable from ocean conditions Fuhrman, J. A.; Hewson, I.; Schwalbach, M. S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 35 https://doi.org/10.1073/pnas.0602399103	journal	August 2006
Qualitative simulation of the carbon starvation response in Escherichia coli Ropers, Delphine; de Jong, Hidde; Page, Michel Biosystems, Vol. 84, Issue 2 https://doi.org/10.1016/j.biosystems.2005.10.005	journal	May 2006
REVIEW: Predictive ecology in a changing world Mouquet, Nicolas; Lagadeuc, Yvan; Devictor, Vincent Journal of Applied Ecology, Vol. 52, Issue 5 https://doi.org/10.1111/1365-2664.12482	journal	July 2015
Large-scale reconstruction and phylogenetic analysis of metabolic environments Borenstein, E.; Kupiec, M.; Feldman, M. W. Proceedings of the National Academy of Sciences, Vol. 105, Issue 38 https://doi.org/10.1073/pnas.0806162105	journal	September 2008
Environmental factors determining ammonia-oxidizing organism distribution and diversity in marine environments: Ammonia-oxidizers across aquatic environmental gradients Bouskill, Nicholas J.; Eveillard, Damien; Chien, Diana Environmental Microbiology, Vol. 14, Issue 3 https://doi.org/10.1111/j.1462-2920.2011.02623.x	journal	November 2011
Comparison of probabilistic Boolean network and dynamic Bayesian network approaches for inferring gene regulatory networks Li, Peng; Zhang, Chaoyang; Perkins, Edward J. BMC Bioinformatics, Vol. 8, Issue Suppl 7 https://doi.org/10.1186/1471-2105-8-S7-S13	journal	January 2007
Metabolic dependencies drive species co-occurrence in diverse microbial communities Zelezniak, Aleksej; Andrejev, Sergej; Ponomarova, Olga Proceedings of the National Academy of Sciences, Vol. 112, Issue 20 https://doi.org/10.1073/pnas.1421834112	journal	May 2015
Putative bacterial interactions from metagenomic knowledge with an integrative systems ecology approach Bordron, Philippe; Latorre, Mauricio; Cortés, Maria-Paz MicrobiologyOpen, Vol. 5, Issue 1 https://doi.org/10.1002/mbo3.315	journal	December 2015
Qualitative simulation of the carbon starvation response in Escherichia coli Ropers, Delphine; de Jong, Hidde; Page, Michel Biosystems, Vol. 84, Issue 2 https://doi.org/10.1016/j.biosystems.2005.10.005	journal	May 2006
Ecosystems biology of microbial metabolism Klitgord, Niels; Segrè, Daniel Current Opinion in Biotechnology, Vol. 22, Issue 4 https://doi.org/10.1016/j.copbio.2011.04.018	journal	August 2011
Multivariate Normal Approximation for the Stochastic Simulation Algorithm: Limit Theorem and Applications Picard, Vincent; Siegel, Anne; Bourdon, Jérémie Electronic Notes in Theoretical Computer Science, Vol. 316 https://doi.org/10.1016/j.entcs.2015.06.011	journal	September 2015
Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer Jewell, Talia N. M.; Karaoz, Ulas; Brodie, Eoin L. The ISME Journal, Vol. 10, Issue 9 https://doi.org/10.1038/ismej.2016.25	journal	March 2016
Toward molecular trait‐based ecology through integration of biogeochemical, geographical and metagenomic data Raes, Jeroen; Letunic, Ivica; Yamada, Takuji Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.6	journal	January 2011
Plankton networks driving carbon export in the oligotrophic ocean Guidi, Lionel; Chaffron, Samuel; Bittner, Lucie Nature, Vol. 532, Issue 7600 https://doi.org/10.1038/nature16942	journal	February 2016
The microbial nitrogen-cycling network Kuypers, Marcel M. M.; Marchant, Hannah K.; Kartal, Boran Nature Reviews Microbiology, Vol. 16, Issue 5 https://doi.org/10.1038/nrmicro.2018.9	journal	February 2018
Molecular eco-systems biology: towards an understanding of community function Raes, Jeroen; Bork, Peer Nature Reviews Microbiology, Vol. 6, Issue 9 https://doi.org/10.1038/nrmicro1935	journal	June 2008
Microbial interactions: from networks to models Faust, Karoline; Raes, Jeroen Nature Reviews Microbiology, Vol. 10, Issue 8 https://doi.org/10.1038/nrmicro2832	journal	July 2012
Metaproteomics reveal that rapid perturbations in organic matter prioritize functional restructuring over taxonomy in western Arctic Ocean microbiomes Mikan, Molly P.; Harvey, H. Rodger; Timmins-Schiffman, Emma The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396-019-0503-z	journal	September 2019
Red versus green leaves: transcriptomic comparison of foliar senescence between two Prunus cerasifera genotypes Vangelisti, Alberto; Guidi, Lucia; Cavallini, Andrea Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-58878-8	journal	February 2020
A Logic for Checking the Probabilistic Steady-State Properties of Reaction Networks Picard, Vincent; Siegel, Anne; Bourdon, Jérémie Journal of Computational Biology, Vol. 24, Issue 8 https://doi.org/10.1089/cmb.2017.0099	journal	August 2017
Probabilistic Boolean networks: a rule-based uncertainty model for gene regulatory networks Shmulevich, I.; Dougherty, E. R.; Kim, S. Bioinformatics, Vol. 18, Issue 2 https://doi.org/10.1093/bioinformatics/18.2.261	journal	February 2002
Analysis of membrane proteins in metagenomics: Networks of correlated environmental features and protein families Patel, P. V.; Gianoulis, T. A.; Bjornson, R. D. Genome Research, Vol. 20, Issue 7 https://doi.org/10.1101/gr.102814.109	journal	April 2010
Ammonia-oxidizing bacterial community composition in estuarine and oceanic environments assessed using a functional gene microarray Ward, Bess B.; Eveillard, Damien; Kirshtein, Julie D. Environmental Microbiology, Vol. 9, Issue 10 https://doi.org/10.1111/j.1462-2920.2007.01371.x	journal	October 2007
On the Power of Uncertainties in Microbial System Modeling: No Need To Hide Them Anymore Delahaye, Benoit; Eveillard, Damien; Bouskill, Nicholas mSystems, Vol. 2, Issue 6 https://doi.org/10.1128/msystems.00169-17	journal	December 2017
Where Next for Microbiome Research? Waldor, Matthew K.; Tyson, Gene; Borenstein, Elhanan PLOS Biology, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pbio.1002050	journal	January 2015
Integrating Quantitative Knowledge into a Qualitative Gene Regulatory Network Bourdon, Jérémie; Eveillard, Damien; Siegel, Anne PLoS Computational Biology, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pcbi.1002157	journal	September 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
Metabolic Network Modeling of Microbial Interactions in Natural and Engineered Environmental Systems Perez-Garcia, Octavio; Lear, Gavin; Singhal, Naresh Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00673	journal	May 2016
Ecological Systems as Complex Systems: Challenges for an Emerging Science Anand, Madhur; Gonzalez, Andrew; Guichard, Frédéric Diversity, Vol. 2, Issue 3 https://doi.org/10.3390/d2030395	journal	March 2010