Deciphering microbial interactions in synthetic human gut microbiome communities

Venturelli, Ophelia S.; Carr, Alex V.; Fisher, Garth; Hsu, Ryan H.; Lau, Rebecca; Bowen, Benjamin P.; Hromada, Susan; Northen, Trent; Arkin, Adam P.

doi:10.15252/msb.20178157

Deciphering microbial interactions in synthetic human gut microbiome communities

Journal Article · Fri Jun 01 00:00:00 EDT 2018 · Molecular Systems Biology

DOI:https://doi.org/10.15252/msb.20178157· OSTI ID:1627937

^[1]; Carr, Alex V. ^[2]; Fisher, Garth ^[2]; ^[3]; Lau, Rebecca ^[2]; Bowen, Benjamin P. ^[2]; Hromada, Susan ^[4]; Northen, Trent ^[2]; Arkin, Adam P. ^[5]

Department of Biochemistry University of Wisconsin‐Madison Madison WI USA; DOE/OSTI
Environmental Genomics and Systems Biology Lawrence Berkeley National Laboratory Berkeley CA USA
California Institute for Quantitative Biosciences University of California Berkeley Berkeley CA USA
Department of Biochemistry University of Wisconsin‐Madison Madison WI USA
Environmental Genomics and Systems Biology Lawrence Berkeley National Laboratory Berkeley CA USA; California Institute for Quantitative Biosciences University of California Berkeley Berkeley CA USA; Department of Bioengineering University of California Berkeley Berkeley CA USA; Energy Biosciences Institute University of California Berkeley Berkeley CA USA

The ecological forces that govern the assembly and stability of the human gut microbiota remain unresolved. We developed a generalizable model-guided framework to predict higher-dimensional consortia from time-resolved measurements of lower-order assemblages. This method was employed to decipher microbial interactions in a diverse human gut microbiome synthetic community. We show that pairwise interactions are major drivers of multi-species community dynamics, as opposed to higher-order interactions. The inferred ecological network exhibits a high proportion of negative and frequent positive interactions. Ecological drivers and responsive recipient species were discovered in the network. Our model demonstrated that a prevalent positive and negative interaction topology enables robust coexistence by implementing a negative feedback loop that balances disparities in monospecies fitness levels. We show that negative interactions could generate history-dependent responses of initial species proportions that frequently do not originate from bistability. Measurements of extracellular metabolites illuminated the metabolic capabilities of monospecies and potential molecular basis of microbial interactions. In sum, these methods defined the ecological roles of major human-associated intestinal species and illuminated design principles of microbial communities.

View Accepted Manuscript (DOE)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627937

Journal Information:: Molecular Systems Biology, Journal Name: Molecular Systems Biology Journal Issue: 6 Vol. 14; ISSN 1744-4292

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (97)

Quantification of the presence and activity of specific microorganisms in nature Jansson, Janet K.; Prosser, James I. Molecular Biotechnology, Vol. 7, Issue 2 https://doi.org/10.1007/bf02761746	journal	April 1997
Microbiology of regressive autism Finegold, Sydney M.; Downes, Julia; Summanen, Paula H. Anaerobe, Vol. 18, Issue 2 https://doi.org/10.1016/j.anaerobe.2011.12.018	journal	April 2012
Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine Ley, Ruth E.; Peterson, Daniel A.; Gordon, Jeffrey I. Cell, Vol. 124, Issue 4 https://doi.org/10.1016/j.cell.2006.02.017	journal	February 2006
Commensal Bacteroides Species Induce Colitis in Host-Genotype-Specific Fashion in a Mouse Model of Inflammatory Bowel Disease Bloom, Seth M.; Bijanki, Vinieth N.; Nava, Gerardo M. Cell Host & Microbe, Vol. 9, Issue 5 https://doi.org/10.1016/j.chom.2011.04.009	journal	May 2011
Eating For Two: How Metabolism Establishes Interspecies Interactions in the Gut Fischbach, Michael A.; Sonnenburg, Justin L. Cell Host & Microbe, Vol. 10, Issue 4 https://doi.org/10.1016/j.chom.2011.10.002	journal	October 2011
Bacteria Come into Focus: New Tools for Visualizing the Microbiota Propheter, Daniel C.; Hooper, Lora V. Cell Host & Microbe, Vol. 18, Issue 4 https://doi.org/10.1016/j.chom.2015.10.004	journal	October 2015
The Gut Microbiome: Connecting Spatial Organization to Function Tropini, Carolina; Earle, Kristen A.; Huang, Kerwyn Casey Cell Host & Microbe, Vol. 21, Issue 4 https://doi.org/10.1016/j.chom.2017.03.010	journal	April 2017
Dysfunctional Families: Clostridium scindens and Secondary Bile Acids Inhibit the Growth of Clostridium difficile Greathouse, K. Leigh; Harris, Curtis C.; Bultman, Scott J. Cell Metabolism, Vol. 21, Issue 1 https://doi.org/10.1016/j.cmet.2014.12.016	journal	January 2015
Dietary Fiber-Induced Improvement in Glucose Metabolism Is Associated with Increased Abundance of Prevotella Kovatcheva-Datchary, Petia; Nilsson, Anne; Akrami, Rozita Cell Metabolism, Vol. 22, Issue 6 https://doi.org/10.1016/j.cmet.2015.10.001	journal	December 2015
Competition, Not Cooperation, Dominates Interactions among Culturable Microbial Species Foster, Kevin R.; Bell, Thomas Current Biology, Vol. 22, Issue 19 https://doi.org/10.1016/j.cub.2012.08.005	journal	October 2012
Gut–brain axis: how the microbiome influences anxiety and depression Foster, Jane A.; McVey Neufeld, Karen-Anne Trends in Neurosciences, Vol. 36, Issue 5 https://doi.org/10.1016/j.tins.2013.01.005	journal	May 2013
Toward defining the autoimmune microbiome for type 1 diabetes Giongo, Adriana; Gano, Kelsey A.; Crabb, David B. The ISME Journal, Vol. 5, Issue 1 https://doi.org/10.1038/ismej.2010.92	journal	July 2010
Abundance and diversity of mucosa-associated hydrogenotrophic microbes in the healthy human colon Nava, Gerardo M.; Carbonero, Franck; Croix, Jennifer A. The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.90	journal	July 2011
Challenges in microbial ecology: building predictive understanding of community function and dynamics Widder, Stefanie; Allen, Rosalind J.; Pfeiffer, Thomas The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.45	journal	March 2016
Diversity, stability and resilience of the human gut microbiota Lozupone, Catherine A.; Stombaugh, Jesse I.; Gordon, Jeffrey I. Nature, Vol. 489, Issue 7415 https://doi.org/10.1038/nature11550	journal	September 2012
Inhibitory interactions promote frequent bistability among competing bacteria Wright, Erik S.; Vetsigian, Kalin H. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11274	journal	April 2016
High-order species interactions shape ecosystem diversity Bairey, Eyal; Kelsic, Eric D.; Kishony, Roy Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12285	journal	August 2016
Gut microbiota, metabolites and host immunity Rooks, Michelle G.; Garrett, Wendy S. Nature Reviews Immunology, Vol. 16, Issue 6 https://doi.org/10.1038/nri.2016.42	journal	May 2016
The resilience of the intestinal microbiota influences health and disease Sommer, Felix; Anderson, Jacqueline Moltzau; Bharti, Richa Nature Reviews Microbiology, Vol. 15, Issue 10 https://doi.org/10.1038/nrmicro.2017.58	journal	June 2017
Bacterial competition: surviving and thriving in the microbial jungle Hibbing, Michael E.; Fuqua, Clay; Parsek, Matthew R. Nature Reviews Microbiology, Vol. 8, Issue 1 https://doi.org/10.1038/nrmicro2259	journal	November 2009
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
The gut microbiota, bacterial metabolites and colorectal cancer Louis, Petra; Hold, Georgina L.; Flint, Harry J. Nature Reviews Microbiology, Vol. 12, Issue 10 https://doi.org/10.1038/nrmicro3344	journal	September 2014
Gut biogeography of the bacterial microbiota Donaldson, Gregory P.; Lee, S. Melanie; Mazmanian, Sarkis K. Nature Reviews Microbiology, Vol. 14, Issue 1 https://doi.org/10.1038/nrmicro3552	journal	October 2015
Mitigating Herding in Hierarchical Crowdsourcing Networks Yu, Han; Miao, Chunyan; Leung, Cyril Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/s41598-016-0011-6	journal	December 2016
Obesity alters gut microbial ecology Ley, R. E.; Backhed, F.; Turnbaugh, P. Proceedings of the National Academy of Sciences, Vol. 102, Issue 31 https://doi.org/10.1073/pnas.0504978102	journal	July 2005
Spatial organization of a model 15-member human gut microbiota established in gnotobiotic mice Mark Welch, Jessica L.; Hasegawa, Yuko; McNulty, Nathan P. Proceedings of the National Academy of Sciences, Vol. 114, Issue 43 https://doi.org/10.1073/pnas.1711596114	journal	October 2017
PEAR: a fast and accurate Illumina Paired-End reAd mergeR Zhang, J.; Kobert, K.; Flouri, T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt593	journal	October 2013
The human microbiome: ecosystem resilience and health Relman, David A. Nutrition Reviews, Vol. 70 https://doi.org/10.1111/j.1753-4887.2012.00489.x	journal	August 2012
Absolute bacterial cell enumeration using flow cytometry Ou, F.; McGoverin, C.; Swift, S. Journal of Applied Microbiology, Vol. 123, Issue 2 https://doi.org/10.1111/jam.13508	journal	July 2017
Predicting and Manipulating Cardiac Drug Inactivation by the Human Gut Bacterium Eggerthella lenta Haiser, H. J.; Gootenberg, D. B.; Chatman, K. Science, Vol. 341, Issue 6143 https://doi.org/10.1126/science.1235872	journal	July 2013
Microbial Interactions within a Cheese Microbial Community Mounier, J.; Monnet, C.; Vallaeys, T. Applied and Environmental Microbiology, Vol. 74, Issue 1 https://doi.org/10.1128/aem.01338-07	journal	November 2007
Intestinal floras of populations that have a high risk of colon cancer. Moore, W. E.; Moore, L. H. Applied and environmental microbiology, Vol. 61, Issue 9 https://doi.org/10.1128/aem.61.9.3202-3207.1995	journal	January 1995
Acetate Utilization and Butyryl Coenzyme A (CoA):Acetate-CoA Transferase in Butyrate-Producing Bacteria from the Human Large Intestine Duncan, S. H.; Barcenilla, A.; Stewart, C. S. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/aem.68.10.5186-5190.2002	journal	October 2002
Coculture of Staphylococcus aureus with Pseudomonas aeruginosa Drives S. aureus towards Fermentative Metabolism and Reduced Viability in a Cystic Fibrosis Model Filkins, Laura M.; Graber, Jyoti A.; Olson, Daniel G. Journal of Bacteriology, Vol. 197, Issue 14 https://doi.org/10.1128/jb.00059-15	journal	April 2015
Butyrate inhibits inflammatory responses through NFkappa B inhibition: implications for Crohn's disease Segain, J-P Gut, Vol. 47, Issue 3 https://doi.org/10.1136/gut.47.3.397	journal	September 2000
Stool consistency is strongly associated with gut microbiota richness and composition, enterotypes and bacterial growth rates Vandeputte, Doris; Falony, Gwen; Vieira-Silva, Sara Gut, Vol. 65, Issue 1 https://doi.org/10.1136/gutjnl-2015-309618	journal	June 2015
Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children De Palma, Giada; Nadal, Inmaculada; Medina, Marcela BMC Microbiology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2180-10-63	journal	January 2010
Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent Wrzosek, Laura; Miquel, Sylvie; Noordine, Marie-Louise BMC Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1741-7007-11-61	journal	January 2013
An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform Fadrosh, Douglas W.; Ma, Bing; Gajer, Pawel Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-6	journal	January 2014
Parameter identifiability analysis and visualization in large-scale kinetic models of biosystems Gábor, Attila; Villaverde, Alejandro F.; Banga, Julio R. BMC Systems Biology, Vol. 11, Issue 1 https://doi.org/10.1186/s12918-017-0428-y	journal	May 2017
Microbial Co-occurrence Relationships in the Human Microbiome Faust, Karoline; Sathirapongsasuti, J. Fah; Izard, Jacques PLoS Computational Biology, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pcbi.1002606	journal	July 2012
The Contribution of High-Order Metabolic Interactions to the Global Activity of a Four-Species Microbial Community Guo, Xiaokan; Boedicker, James Q. PLOS Computational Biology, Vol. 12, Issue 9 https://doi.org/10.1371/journal.pcbi.1005079	journal	September 2016
Gut Microbiota in Human Adults with Type 2 Diabetes Differs from Non-Diabetic Adults Larsen, Nadja; Vogensen, Finn K.; van den Berg, Frans W. J. PLoS ONE, Vol. 5, Issue 2 https://doi.org/10.1371/journal.pone.0009085	journal	February 2010
Bacteroides uniformis CECT 7771 Ameliorates Metabolic and Immunological Dysfunction in Mice with High-Fat-Diet Induced Obesity Gauffin Cano, Paola; Santacruz, Arlette; Moya, Ángela PLoS ONE, Vol. 7, Issue 7 https://doi.org/10.1371/journal.pone.0041079	journal	July 2012
Reduced Incidence of Prevotella and Other Fermenters in Intestinal Microflora of Autistic Children Kang, Dae-Wook; Park, Jin Gyoon; Ilhan, Zehra Esra PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0068322	journal	July 2013
Eggerthella lenta bacteremia in a Crohn’s disease patient after ileocecal resection Thota, Venkata R.; Dacha, Sunil; Natarajan, Aparna Future Microbiology, Vol. 6, Issue 5 https://doi.org/10.2217/fmb.11.31	journal	May 2011
Analysis of Metabolomics Datasets with High-Performance Computing and Metabolite Atlases Yao, Yushu; Sun, Terence; Wang, Tony Metabolites, Vol. 5, Issue 3 https://doi.org/10.3390/metabo5030431	journal	July 2015
Condition-dependent cell volume and concentration of Escherichia coli to facilitate data conversion for systems biology modeling Volkmer, Benjamin; Heinemann, Matthias ETH Zurich https://doi.org/10.3929/ethz-b-000038570	text	January 2011
Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis Scher, Jose U.; Sczesnak, Andrew; Longman, Randy S. eLife, Vol. 2 https://doi.org/10.7554/elife.01202	journal	November 2013
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014
Quantification of the presence and activity of specific microorganisms in nature Jansson, Janet K.; Prosser, James I. Molecular Biotechnology, Vol. 7, Issue 2 https://doi.org/10.1007/BF02761746	journal	April 1997
Bifidobacterium Lactis Probio-M8 regulates gut microbiota to alleviate Alzheimer’s disease in the APP/PS1 mouse model Cao, Jianing; Amakye, William Kwame; Qi, Chunli European Journal of Nutrition https://doi.org/10.1007/s00394-021-02543-x	journal	April 2021
Mathematical biology Ermentrout, Bard Mathematical Biosciences, Vol. 103, Issue 1 https://doi.org/10.1016/0025-5564(91)90096-2	journal	February 1991
Quantitative Imaging of Gut Microbiota Spatial Organization Earle, Kristen A.; Billings, Gabriel; Sigal, Michael Cell Host & Microbe, Vol. 18, Issue 4 https://doi.org/10.1016/j.chom.2015.09.002	journal	October 2015
Specialized Metabolites from the Microbiome in Health and Disease Sharon, Gil; Garg, Neha; Debelius, Justine Cell Metabolism, Vol. 20, Issue 5 https://doi.org/10.1016/j.cmet.2014.10.016	journal	November 2014
A human gut microbial gene catalogue established by metagenomic sequencing Qin, Junjie; Li, Ruiqiang; Raes, Jeroen Nature, Vol. 464, Issue 7285 https://doi.org/10.1038/nature08821	journal	March 2010
Ecological interactions are evolutionarily conserved across the entire tree of life Gómez, José M.; Verdú, Miguel; Perfectti, Francisco Nature, Vol. 465, Issue 7300 https://doi.org/10.1038/nature09113	journal	June 2010
Enterotypes of the human gut microbiome Arumugam, Manimozhiyan; Raes, Jeroen; Pelletier, Eric Nature, Vol. 473, Issue 7346 https://doi.org/10.1038/nature09944	journal	April 2011
Precision microbiome reconstitution restores bile acid mediated resistance to Clostridium difficile Buffie, Charlie G.; Bucci, Vanni; Stein, Richard R. Nature, Vol. 517, Issue 7533 https://doi.org/10.1038/nature13828	journal	October 2014
Universality of human microbial dynamics Bashan, Amir; Gibson, Travis E.; Friedman, Jonathan Nature, Vol. 534, Issue 7606 https://doi.org/10.1038/nature18301	journal	June 2016
Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut Roager, Henrik M.; Hansen, Lea B. S.; Bahl, Martin I. Nature Microbiology, Vol. 1, Issue 9 https://doi.org/10.1038/nmicrobiol.2016.93	journal	June 2016
Prevotella in the gut: choose carefully Ley, Ruth E. Nature Reviews Gastroenterology & Hepatology, Vol. 13, Issue 2 https://doi.org/10.1038/nrgastro.2016.4	journal	February 2016
Biogeographical patterns and mechanisms of microbial community assembly that underlie successional biocrusts across northern China Li, Yuanlong; Hu, Chunxiang npj Biofilms and Microbiomes, Vol. 7, Issue 1 https://doi.org/10.1038/s41522-021-00188-6	journal	February 2021
Community structure follows simple assembly rules in microbial microcosms Friedman, Jonathan; Higgins, Logan M.; Gore, Jeff Nature Ecology & Evolution, Vol. 1, Issue 5 https://doi.org/10.1038/s41559-017-0109	journal	March 2017
General calibration of microbial growth in microplate readers Stevenson, Keiran; McVey, Alexander F.; Clark, Ivan B. N. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep38828	journal	December 2016
Feedback systems Pedersen, F. Beam dynamics issues of high luminosity asymmetric collider rings, AIP Conference Proceedings https://doi.org/10.1063/1.39774	conference	January 1990
Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients Sokol, H.; Pigneur, B.; Watterlot, L. Proceedings of the National Academy of Sciences, Vol. 105, Issue 43 https://doi.org/10.1073/pnas.0804812105	journal	October 2008
Interaction networks, ecological stability, and collective antibiotic tolerance in polymicrobial infections de Vos, Marjon G. J.; Zagorski, Marcin; McNally, Alan Proceedings of the National Academy of Sciences, Vol. 114, Issue 40 https://doi.org/10.1073/pnas.1713372114	journal	September 2017
Enhanced butyrate formation by cross-feeding between Faecalibacterium prausnitzii and Bifidobacterium adolescentis Rios-Covian, David; Gueimonde, Miguel; Duncan, Sylvia H. FEMS Microbiology Letters, Vol. 362, Issue 21 https://doi.org/10.1093/femsle/fnv176	journal	September 2015
BiMat: a MATLAB package to facilitate the analysis of bipartite networks Flores, Cesar O.; Poisot, Timothée; Valverde, Sergi Methods in Ecology and Evolution, Vol. 7, Issue 1 https://doi.org/10.1111/2041-210X.12458	journal	August 2015
Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn's disease: Abundance of Faecalibacterium prausnitzii Fujimoto, Takehide; Imaeda, Hirotsugu; Takahashi, Kenichiro Journal of Gastroenterology and Hepatology, Vol. 28, Issue 4 https://doi.org/10.1111/jgh.12073	journal	March 2013
Diversity of Interaction Types and Ecological Community Stability Mougi, A.; Kondoh, M. Science, Vol. 337, Issue 6092 https://doi.org/10.1126/science.1220529	journal	July 2012
The Long-Term Stability of the Human Gut Microbiota Faith, Jeremiah J.; Guruge, Janaki L.; Charbonneau, Mark Science, Vol. 341, Issue 6141 https://doi.org/10.1126/science.1237439	journal	July 2013
The ecology of the microbiome: Networks, competition, and stability Coyte, K. Z.; Schluter, J.; Foster, K. R. Science, Vol. 350, Issue 6261 https://doi.org/10.1126/science.aad2602	journal	November 2015
Microbial Interactions within a Cheese Microbial Community Mounier, J.; Monnet, C.; Vallaeys, T. Applied and Environmental Microbiology, Vol. 74, Issue 1 https://doi.org/10.1128/AEM.01338-07	journal	November 2007
Intestinal floras of populations that have a high risk of colon cancer. Moore, W. E.; Moore, L. H. Applied and environmental microbiology, Vol. 61, Issue 9 https://doi.org/10.1128/AEM.61.9.3202-3207.1995	journal	January 1995
Acetate Utilization and Butyryl Coenzyme A (CoA):Acetate-CoA Transferase in Butyrate-Producing Bacteria from the Human Large Intestine Duncan, S. H.; Barcenilla, A.; Stewart, C. S. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/AEM.68.10.5186-5190.2002	journal	October 2002
Coculture of Staphylococcus aureus with Pseudomonas aeruginosa Drives S. aureus towards Fermentative Metabolism and Reduced Viability in a Cystic Fibrosis Model Filkins, Laura M.; Graber, Jyoti A.; Olson, Daniel G. Journal of Bacteriology, Vol. 197, Issue 14 https://doi.org/10.1128/JB.00059-15	journal	April 2015
MDSINE: Microbial Dynamical Systems INference Engine for microbiome time-series analyses Bucci, Vanni; Tzen, Belinda; Li, Ning Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-0980-6	journal	June 2016
An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis Chen, Jun; Wright, Kerry; Davis, John M. Genome Medicine, Vol. 8, Issue 1 https://doi.org/10.1186/s13073-016-0299-7	journal	April 2016
Ecological Modeling from Time-Series Inference: Insight into Dynamics and Stability of Intestinal Microbiota Stein, Richard R.; Bucci, Vanni; Toussaint, Nora C. PLoS Computational Biology, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pcbi.1003388	journal	December 2013
On the Origins and Control of Community Types in the Human Microbiome Gibson, Travis E.; Bashan, Amir; Cao, Hong-Tai PLOS Computational Biology, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pcbi.1004688	journal	February 2016
Condition-Dependent Cell Volume and Concentration of Escherichia coli to Facilitate Data Conversion for Systems Biology Modeling Volkmer, Benjamin; Heinemann, Matthias PLoS ONE, Vol. 6, Issue 7 https://doi.org/10.1371/journal.pone.0023126	journal	July 2011
Identifying Keystone Species in the Human Gut Microbiome from Metagenomic Timeseries Using Sparse Linear Regression Fisher, Charles K.; Mehta, Pankaj PLoS ONE, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pone.0102451	journal	July 2014
Mathematical Biology Oberwolfach, Mathematisches Forschungsinstitut Mathematisches Forschungsinstitut Oberwolfach https://doi.org/10.14760/owr-2006-24	text	January 2006
Challenges in microbial ecology: building predictive understanding of community function and dynamics. Widder, Stefanie; Allen, Rosalind J.; Allen, Rosalind J. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.10735	text	January 2016
Permanence and the Assembly of Ecological Communities Law, Richard; Morton, R. Daniel Ecology, Vol. 77, Issue 3 https://doi.org/10.2307/2265500	journal	April 1996
Challenges in microbial ecology: Building predictive understanding of community function and dynamics No authors listed My University https://doi.org/10.34944/dspace/5051	text	January 2016
Identifying Keystone Species in the Human Gut Microbiome from Metagenomic Timeseries using Sparse Linear Regression Fisher, Charles K.; Mehta, Pankaj arXiv https://doi.org/10.48550/arxiv.1402.0511	text	January 2014
Absolute bacterial cell enumeration using flow cytometry Ou, Fang; McGoverin, Cushla; Swift, Simon arXiv https://doi.org/10.48550/arxiv.1703.00895	text	January 2017
PhyloSift: Phylogenetic analysis of genomes and metagenomes Bik, Holly; Matsen, Erick; Lowe, Eric Figshare https://doi.org/10.6084/m9.figshare.706369	dataset	January 2013
PhyloSift: Phylogenetic analysis of genomes and metagenomes Bik, Holly; Matsen, Erick; Lowe, Eric figshare https://doi.org/10.6084/m9.figshare.706369.v1	dataset	January 2013
MDSINE: Microbial Dynamical Systems INference Engine for microbiome time-series analyses Bucci, Vanni; Tzen, Belinda; Li, Ning figshare https://doi.org/10.6084/m9.figshare.c.3640829	collection	January 2016
An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis Chen, Jun; Wright, Kerry; Davis, John figshare https://doi.org/10.6084/m9.figshare.c.3645932	collection	January 2016
Parameter identifiability analysis and visualization in large-scale kinetic models of biosystems Gรกbor, Attila; Villaverde, Alejandro F.; Banga, Julio R. Figshare https://doi.org/10.6084/m9.figshare.c.3772991	collection	January 2017
Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis Scher, Jose U.; Sczesnak, Andrew; Longman, Randy S. eLife, Vol. 2 https://doi.org/10.7554/eLife.01202	journal	November 2013
Lotka-Volterra pairwise modeling fails to capture diverse pairwise microbial interactions Momeni, Babak; Xie, Li; Shou, Wenying eLife, Vol. 6 https://doi.org/10.7554/eLife.25051	journal	March 2017

Cited By (32)

Rhizobacteria Mediate the Phytotoxicity of a Range of Biorefinery‐Relevant Compounds Herbert, Robin A.; Eng, Thomas; Martinez, Uriel Environmental Toxicology and Chemistry, Vol. 38, Issue 9 https://doi.org/10.1002/etc.4501	journal	July 2019
The Human Gut Microbiome is Structured to Optimize Molecular Interaction Networks Ling, Yiwei; Watanabe, Yu; Okuda, Shujiro Computational and Structural Biotechnology Journal, Vol. 17 https://doi.org/10.1016/j.csbj.2019.07.011	journal	January 2019
Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere Carlström, Charlotte I.; Field, Christopher M.; Bortfeld-Miller, Miriam Nature Ecology & Evolution, Vol. 3, Issue 10 https://doi.org/10.1038/s41559-019-0994-z	journal	September 2019
A multidimensional perspective on microbial interactions Pacheco, Alan R.; Segrè, Daniel FEMS Microbiology Letters, Vol. 366, Issue 11 https://doi.org/10.1093/femsle/fnz125	journal	June 2019
Interrogation of Internal Workings in Microbial Community Assembly: Play a Game through a Behavioral Network? Wang, Qian; Liu, Xinjuan; Jiang, Libo mSystems, Vol. 4, Issue 5 https://doi.org/10.1128/msystems.00550-19	journal	October 2019
Difficulty in inferring microbial community structure based on co-occurrence network approaches Hirano, Hokuto; Takemoto, Kazuhiro BMC Bioinformatics, Vol. 20, Issue 1 https://doi.org/10.1186/s12859-019-2915-1	journal	June 2019
Enhanced inference of ecological networks by parameterizing ensembles of population dynamics models constrained with prior knowledge Liao, Chen; Xavier, Joao B.; Zhu, Zhenduo BMC Ecology, Vol. 20, Issue 1 https://doi.org/10.1186/s12898-019-0272-6	journal	January 2020
High-order interactions distort the functional landscape of microbial consortia Sanchez-Gorostiaga, Alicia; Bajić, Djordje; Osborne, Melisa L. PLOS Biology, Vol. 17, Issue 12 https://doi.org/10.1371/journal.pbio.3000550	journal	December 2019
Available energy fluxes drive a transition in the diversity, stability, and functional structure of microbial communities Marsland, Robert; Cui, Wenping; Goldford, Joshua PLOS Computational Biology, Vol. 15, Issue 2 https://doi.org/10.1371/journal.pcbi.1006793	journal	February 2019
Web-gLV: A Web Based Platform for Lotka-Volterra Based Modeling and Simulation of Microbial Populations Kuntal, Bhusan K.; Gadgil, Chetan; Mande, Sharmila S. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00288	journal	February 2019
Efficient engineered probiotics using synthetic biology approaches: A review Yadav, Monika; Shukla, Pratyoosh Biotechnology and Applied Biochemistry, Vol. 67, Issue 1 https://doi.org/10.1002/bab.1822	journal	January 2020
Characterize carbapenem-resistant Klebsiella pneumoniae isolates for nosocomial pneumonia and their Gram-negative bacteria neighbors in the respiratory tract Zhao, Dongmei; Zuo, Yan; Wang, Zhongxin Molecular Biology Reports, Vol. 46, Issue 1 https://doi.org/10.1007/s11033-018-4515-y	journal	January 2019
Multiple stable states in microbial communities explained by the stable marriage problem Goyal, Akshit; Dubinkina, Veronika; Maslov, Sergei The ISME Journal, Vol. 12, Issue 12 https://doi.org/10.1038/s41396-018-0222-x	journal	July 2018
Modelling microbiome recovery after antibiotics using a stability landscape framework Shaw, Liam P.; Bassam, Hassan; Barnes, Chris P. The ISME Journal, Vol. 13, Issue 7 https://doi.org/10.1038/s41396-019-0392-1	journal	March 2019
Use and abuse of correlation analyses in microbial ecology Carr, Alex; Diener, Christian; Baliga, Nitin S. The ISME Journal, Vol. 13, Issue 11 https://doi.org/10.1038/s41396-019-0459-z	journal	June 2019
Mortality causes universal changes in microbial community composition Abreu, Clare I.; Friedman, Jonathan; Andersen Woltz, Vilhelm L. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09925-0	journal	May 2019
Microbial coexistence through chemical-mediated interactions Niehaus, Lori; Boland, Ian; Liu, Minghao Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10062-x	journal	May 2019
Modelling approaches for studying the microbiome Kumar, Manish; Ji, Boyang; Zengler, Karsten Nature Microbiology, Vol. 4, Issue 8 https://doi.org/10.1038/s41564-019-0491-9	journal	July 2019
Common principles and best practices for engineering microbiomes Lawson, Christopher E.; Harcombe, William R.; Hatzenpichler, Roland Nature Reviews Microbiology, Vol. 17, Issue 12 https://doi.org/10.1038/s41579-019-0255-9	journal	September 2019
Synthetic ecology of the human gut microbiota Vrancken, Gino; Gregory, Ann C.; Huys, Geert R. B. Nature Reviews Microbiology, Vol. 17, Issue 12 https://doi.org/10.1038/s41579-019-0264-8	journal	October 2019
Massively parallel screening of synthetic microbial communities Kehe, Jared; Kulesa, Anthony; Ortiz, Anthony Proceedings of the National Academy of Sciences, Vol. 116, Issue 26 https://doi.org/10.1073/pnas.1900102116	journal	June 2019
Immigration-induced phase transition in a regulated multispecies birth-death process Xu, Song; Chou, Tom Journal of Physics A: Mathematical and Theoretical, Vol. 51, Issue 42 https://doi.org/10.1088/1751-8121/aadcb4	journal	September 2018
Can dynamic network modelling be used to identify adaptive microbiomes? Garcia, Joshua; Kao‐Kniffin, Jenny Functional Ecology, Vol. 34, Issue 10 https://doi.org/10.1111/1365-2435.13491	journal	December 2019
Contrasting Strategies: Human Eukaryotic Versus Bacterial Microbiome Research Hooks, Katarzyna B.; O'Malley, Maureen A. Journal of Eukaryotic Microbiology, Vol. 67, Issue 2 https://doi.org/10.1111/jeu.12766	journal	October 2019
Metabolic Basis for Mutualism between Gut Bacteria and Its Impact on the Drosophila melanogaster Host Sommer, Andrew J.; Newell, Peter D. Applied and Environmental Microbiology, Vol. 85, Issue 2 https://doi.org/10.1128/aem.01882-18	journal	November 2018
Introducing THOR, a Model Microbiome for Genetic Dissection of Community Behavior Lozano, Gabriel L.; Bravo, Juan I.; Garavito Diago, Manuel F. mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mbio.02846-18	journal	March 2019
Towards a Better Understanding of Microbial Community Dynamics through High-Throughput Cultivation and Data Integration Faust, Karoline mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/msystems.00101-19	journal	May 2019
Species Deletions from Microbiome Consortia Reveal Key Metabolic Interactions between Gut Microbes Gutiérrez, Natalia; Garrido, Daniel mSystems, Vol. 4, Issue 4 https://doi.org/10.1128/msystems.00185-19	journal	July 2019
An expectation-maximization algorithm enables accurate ecological modeling using longitudinal microbiome sequencing data Li, Chenhao; Chng, Kern Rei; Kwah, Junmei Samantha Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0729-z	journal	August 2019
Scalable nonlinear programming framework for parameter estimation in dynamic biological system models Shin, Sungho; Venturelli, Ophelia S.; Zavala, Victor M. PLOS Computational Biology, Vol. 15, Issue 3 https://doi.org/10.1371/journal.pcbi.1006828	journal	March 2019
Pairing off: a bottom‐up approach to the human gut microbiome Abreu, Clare; Ortiz Lopez, Anthony; Gore, Jeff Molecular Systems Biology, Vol. 14, Issue 6 https://doi.org/10.15252/msb.20188425	journal	June 2018
Immigration-induced phase transition in a regulated multispecies birth-death process Xu, Song; Chou, Tom arXiv https://doi.org/10.48550/arxiv.1808.08948	text	January 2018

Similar Records

The gut mycobiota of rural and urban individuals is shaped by geography

Journal Article · Sun Aug 16 20:00:00 EDT 2020 · BMC Microbiology · OSTI ID:1668324

Exposing new taxonomic variation with inflammation — a murine model-specific genome database for gut microbiome researchers

Journal Article · Fri May 19 20:00:00 EDT 2023 · Microbiome · OSTI ID:2422515

Related Subjects

Biochemistry & Molecular Biology

Deciphering microbial interactions in synthetic human gut microbiome communities

Citation Formats

References (97)

Cited By (32)

Similar Records

Related Subjects