Interaction variability shapes succession of synthetic microbial ecosystems

Liu, Feng; Mao, Junwen; Kong, Wentao; Hua, Qiang; Feng, Youjun; Bashir, Rashid; Lu, Ting

doi:10.1038/s41467-019-13986-6

Interaction variability shapes succession of synthetic microbial ecosystems

Journal Article · Thu Jan 16 00:00:00 UTC 2020 · Nature Communications

DOI:https://doi.org/10.1038/s41467-019-13986-6· OSTI ID:1619730

Liu, Feng; Mao, Junwen; Kong, Wentao; Hua, Qiang; Feng, Youjun; Bashir, Rashid; Lu, Ting

Abstract

Cellular interactions are a major driver for the assembly and functioning of microbial communities. Their strengths are shown to be highly variable in nature; however, it is unclear how such variations regulate community behaviors. Here we construct synthetic Lactococcus lactis consortia and mathematical models to elucidate the role of interaction variability in ecosystem succession and to further determine if casting variability into modeling empowers bottom-up predictions. For a consortium of bacteriocin-mediated cooperation and competition, we find increasing the variations of cooperation, from either altered labor partition or random sampling, drives the community into distinct structures. When the cooperation and competition are additionally modulated by pH, ecosystem succession becomes jointly controlled by the variations of both interactions and yields more diversified dynamics. Mathematical models incorporating variability successfully capture all of these experimental observations. Our study demonstrates interaction variability as a key regulator of community dynamics, providing insights into bottom-up predictions of microbial ecosystems.

View Journal Article

Research Organization:: University of Illinois at Urbana-Champaign

Sponsoring Organization:: China Scholarship Council; National Natural Science Foundation of China (NSFC); National Science Foundation (NSF); US Department of the Navy, Office of Naval Research (ONR); USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0019185

OSTI ID:: 1619730

Alternate ID(s):: OSTI ID: 1595091

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 11; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (69)

Plasmid-encoded protein: The principal factor in the “metabolic burden” associated with recombinant bacteria Bentley, William E.; Mirjalili, Noushin; Andersen, Dana C. Biotechnology and Bioengineering, Vol. 35, Issue 7 https://doi.org/10.1002/bit.260350704	journal	March 1990
Modeling Microbial Dynamics in Heterogeneous Environments: Growth on Soil Carbon Sources Resat, Haluk; Bailey, Vanessa; McCue, Lee Ann Microbial Ecology, Vol. 63, Issue 4 https://doi.org/10.1007/s00248-011-9965-x	journal	December 2011
Metabolic load and heterologous gene expression Glick, Bernard R. Biotechnology Advances, Vol. 13, Issue 2 https://doi.org/10.1016/0734-9750(95)00004-A	journal	January 1995
Population balance modeling. Promise for the future Ramkrishna, Doraiswami; Mahoney, Alan W. Chemical Engineering Science, Vol. 57, Issue 4 https://doi.org/10.1016/S0009-2509(01)00386-4	journal	February 2002
Microbiome therapeutics — Advances and challenges Mimee, Mark; Citorik, Robert J.; Lu, Timothy K. Advanced Drug Delivery Reviews, Vol. 105 https://doi.org/10.1016/j.addr.2016.04.032	journal	October 2016
Genetic drift Masel, Joanna Current Biology, Vol. 21, Issue 20 https://doi.org/10.1016/j.cub.2011.08.007	journal	October 2011
A bunch of tiny individuals—Individual-based modeling for microbes Hellweger, Ferdi L.; Bucci, Vanni Ecological Modelling, Vol. 220, Issue 1 https://doi.org/10.1016/j.ecolmodel.2008.09.004	journal	January 2009
Modification of Lactobacillus β-glucuronidase activity by random mutagenesis Callanan, Michael J.; Russell, William M.; Klaenhammer, Todd R. Gene, Vol. 389, Issue 2 https://doi.org/10.1016/j.gene.2006.10.022	journal	March 2007
Synthetic Ecology of Microbes: Mathematical Models and Applications Zomorrodi, Ali R.; Segrè, Daniel Journal of Molecular Biology, Vol. 428, Issue 5 https://doi.org/10.1016/j.jmb.2015.10.019	journal	February 2016
Synthetic microbial communities Großkopf, Tobias; Soyer, Orkun S. Current Opinion in Microbiology, Vol. 18 https://doi.org/10.1016/j.mib.2014.02.002	journal	April 2014
Principles for designing synthetic microbial communities Johns, Nathan I.; Blazejewski, Tomasz; Gomes, Antonio LC Current Opinion in Microbiology, Vol. 31 https://doi.org/10.1016/j.mib.2016.03.010	journal	June 2016
Microbial interactions and community assembly at microscales Cordero, Otto X.; Datta, Manoshi S. Current Opinion in Microbiology, Vol. 31 https://doi.org/10.1016/j.mib.2016.03.015	journal	June 2016
Microbial communities as dynamical systems Gonze, Didier; Coyte, Katharine Z.; Lahti, Leo Current Opinion in Microbiology, Vol. 44 https://doi.org/10.1016/j.mib.2018.07.004	journal	August 2018
Cellular cooperation: insights from microbes Celiker, Hasan; Gore, Jeff Trends in Cell Biology, Vol. 23, Issue 1 https://doi.org/10.1016/j.tcb.2012.08.010	journal	January 2013
Engineering microbial consortia: a new frontier in synthetic biology Brenner, Katie; You, Lingchong; Arnold, Frances H. Trends in Biotechnology, Vol. 26, Issue 9, p. 483-489 https://doi.org/10.1016/j.tibtech.2008.05.004	journal	September 2008
The rhizosphere microbiome and plant health Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M. Trends in Plant Science, Vol. 17, Issue 8 https://doi.org/10.1016/j.tplants.2012.04.001	journal	August 2012
High-level coproduction of the bacteriocins nisin A and lactococcin A by Lactococcus lactis Fernández, Antonio; Horn, Nikki; Gasson, Michael J. Journal of Dairy Research, Vol. 71, Issue 2 https://doi.org/10.1017/S0022029904000123	journal	May 2004
Synthetic, Context-Dependent Microbial Consortium of Predator and Prey Liu, Feng; Mao, Junwen; Lu, Ting ACS Synthetic Biology, Vol. 8, Issue 8 https://doi.org/10.1021/acssynbio.9b00110	journal	July 2019
Ecology and Evolution of Communities Cody, Martin L.; Diamond, Jared M. Nature, Vol. 260, Issue 5548 https://doi.org/10.1038/260204c0	journal	March 1976
Microbial ecology of biological invasions van der Putten, Wim H.; Klironomos, John N.; Wardle, David A. The ISME Journal, Vol. 1, Issue 1 https://doi.org/10.1038/ismej.2007.9	journal	May 2007
High local substrate availability stabilizes a cooperative trait Bachmann, Herwig; Molenaar, Douwe; Kleerebezem, Michiel The ISME Journal, Vol. 5, Issue 5 https://doi.org/10.1038/ismej.2010.179	journal	December 2010
Stochastic and deterministic assembly processes in subsurface microbial communities Stegen, James C.; Lin, Xueju; Konopka, Allan E. The ISME Journal, Vol. 6, Issue 9 https://doi.org/10.1038/ismej.2012.22	journal	March 2012
Eco-evolutionary feedbacks drive species interactions Andrade-Domínguez, Andrés; Salazar, Emmanuel; del Carmen Vargas-Lagunas, María The ISME Journal, Vol. 8, Issue 5 https://doi.org/10.1038/ismej.2013.208	journal	December 2013
Resource-dependent attenuation of species interactions during bacterial succession Rivett, Damian W.; Scheuerl, Thomas; Culbert, Christopher T. The ISME Journal, Vol. 10, Issue 9 https://doi.org/10.1038/ismej.2016.11	journal	February 2016
Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients LaSarre, Breah; McCully, Alexandra L.; Lennon, Jay T. The ISME Journal, Vol. 11, Issue 2 https://doi.org/10.1038/ismej.2016.141	journal	November 2016
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
A synthetic Escherichia coli predator–prey ecosystem Balagaddé, Frederick K.; Song, Hao; Ozaki, Jun Molecular Systems Biology, Vol. 4, Issue 1 https://doi.org/10.1038/msb.2008.24	journal	January 2008
Emergent cooperation in microbial metabolism Wintermute, Edwin H.; Silver, Pamela A. Molecular Systems Biology, Vol. 6, Issue 1 https://doi.org/10.1038/msb.2010.66	journal	January 2010
Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors Kerr, Benjamin; Riley, Margaret A.; Feldman, Marcus W. Nature, Vol. 418, Issue 6894 https://doi.org/10.1038/nature00823	journal	July 2002
Snowdrift game dynamics and facultative cheating in yeast Gore, Jeff; Youk, Hyun; van Oudenaarden, Alexander Nature, Vol. 459, Issue 7244 https://doi.org/10.1038/nature07921	journal	April 2009
Stochasticity of metabolism and growth at the single-cell level Kiviet, Daniel J.; Nghe, Philippe; Walker, Noreen Nature, Vol. 514, Issue 7522 https://doi.org/10.1038/nature13582	journal	September 2014
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
Chemical decay of an antibiotic inverts selection for resistance Palmer, Adam C.; Angelino, Elaine; Kishony, Roy Nature Chemical Biology, Vol. 6, Issue 2 https://doi.org/10.1038/nchembio.289	journal	January 2010
The role of physiological heterogeneity in microbial population behavior Lidstrom, Mary E.; Konopka, Michael C. Nature Chemical Biology, Vol. 6, Issue 10 https://doi.org/10.1038/nchembio.436	journal	September 2010
Stochasticity in gene expression: from theories to phenotypes Kærn, Mads; Elston, Timothy C.; Blake, William J. Nature Reviews Genetics, Vol. 6, Issue 6 https://doi.org/10.1038/nrg1615	journal	May 2005
The human microbiome: at the interface of health and disease Cho, Ilseung; Blaser, Martin J. Nature Reviews Genetics, Vol. 13, Issue 4 https://doi.org/10.1038/nrg3182	journal	March 2012
Social evolution theory for microorganisms West, Stuart A.; Griffin, Ashleigh S.; Gardner, Andy Nature Reviews Microbiology, Vol. 4, Issue 8 https://doi.org/10.1038/nrmicro1461	journal	August 2006
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
Molecular characterization of the pH-inducible and growth phase-dependent promoter P170 of Lactococcus lactis Madsen, Soren M.; Arnau, Jose; Vrang, Astrid Molecular Microbiology, Vol. 32, Issue 1 https://doi.org/10.1046/j.1365-2958.1999.01326.x	journal	April 1999
Synthetic cooperation in engineered yeast populations Shou, W.; Ram, S.; Vilar, J. M. G. Proceedings of the National Academy of Sciences, Vol. 104, Issue 6 https://doi.org/10.1073/pnas.0610575104	journal	January 2007
Genetic drift at expanding frontiers promotes gene segregation Hallatschek, O.; Hersen, P.; Ramanathan, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 50 https://doi.org/10.1073/pnas.0710150104	journal	December 2007
Fine-tuning gene networks using simple sequence repeats Egbert, R. G.; Klavins, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 42 https://doi.org/10.1073/pnas.1205693109	journal	August 2012
Mathematical modeling of primary succession of murine intestinal microbiota Marino, S.; Baxter, N. T.; Huffnagle, G. B. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1311322111	journal	December 2013
Syntrophic exchange in synthetic microbial communities Mee, M. T.; Collins, J. J.; Church, G. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 20 https://doi.org/10.1073/pnas.1405641111	journal	April 2014
Changes in temperature alter the relationship between biodiversity and ecosystem functioning García, Francisca C.; Bestion, Elvire; Warfield, Ruth Proceedings of the National Academy of Sciences, Vol. 115, Issue 43 https://doi.org/10.1073/pnas.1805518115	journal	October 2018
Autoregulation of Nisin Biosynthesis in Lactococcus lactis by Signal Transduction Kuipers, Oscar P.; Beerthuyzen, Marke M.; de Ruyter, Pascalle G. G. A. Journal of Biological Chemistry, Vol. 270, Issue 45 https://doi.org/10.1074/jbc.270.45.27299	journal	November 1995
Isolation of strong constitutive promoters from Lactococcus lactis subsp. lactis N8 Zhu, Duolong; Liu, Fulu; Xu, Haijin FEMS Microbiology Letters, Vol. 362, Issue 16 https://doi.org/10.1093/femsle/fnv107	journal	July 2015
A gene network engineering platform for lactic acid bacteria Kong, Wentao; Kapuganti, Venkata S.; Lu, Ting Nucleic Acids Research, Vol. 44, Issue 4 https://doi.org/10.1093/nar/gkv1093	journal	October 2015
Differential response of Streptococcus mutans towards friend and foe in mixed-species cultures Liu, J.; Wu, C.; Huang, I. -H. Microbiology, Vol. 157, Issue 9 https://doi.org/10.1099/mic.0.048314-0	journal	May 2011
Spatial interference scale as a determinant of microbial range expansion Celik Ozgen, Venhar; Kong, Wentao; Blanchard, Andrew E. Science Advances, Vol. 4, Issue 11 https://doi.org/10.1126/sciadv.aau0695	journal	November 2018
Stochastic Gene Expression in a Single Cell Elowitz, M. B. Science, Vol. 297, Issue 5584 https://doi.org/10.1126/science.1070919	journal	August 2002
Enterococcus faecalis Senses Target Cells and in Response Expresses Cytolysin Coburn, P. S. Science, Vol. 306, Issue 5705 https://doi.org/10.1126/science.1103996	journal	December 2004
The Microbial Engines That Drive Earth's Biogeochemical Cycles Falkowski, P. G.; Fenchel, T.; Delong, E. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1153213	journal	May 2008
Simpson's Paradox in a Synthetic Microbial System Chuang, J. S.; Rivoire, O.; Leibler, S. Science, Vol. 323, Issue 5911 https://doi.org/10.1126/science.1166739	journal	January 2009
Secreting and Sensing the Same Molecule Allows Cells to Achieve Versatile Social Behaviors Youk, H.; Lim, W. A. Science, Vol. 343, Issue 6171 https://doi.org/10.1126/science.1242782	journal	February 2014
ECOLOGY:How Do Communities Come Together? Gotelli, N. J. Science, Vol. 286, Issue 5445 https://doi.org/10.1126/science.286.5445.1684a	journal	November 1999
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
Lactococcus lactis LMG2081 Produces Two Bacteriocins, a Nonlantibiotic and a Novel Lantibiotic Mirkovic, Nemanja; Polovic, Natalija; Vukotic, Goran Applied and Environmental Microbiology, Vol. 82, Issue 8 https://doi.org/10.1128/AEM.03988-15	journal	February 2016
Iron Depletion Enhances Production of Antimicrobials by Pseudomonas aeruginosa Nguyen, Angela T.; Jones, Jace W.; Ruge, Max A. Journal of Bacteriology, Vol. 197, Issue 14 https://doi.org/10.1128/JB.00072-15	journal	April 2015
Lactococcin G is a potassium ion-conducting, two-component bacteriocin. Moll, G.; Ubbink-Kok, T.; Hildeng-Hauge, H. Journal of bacteriology, Vol. 178, Issue 3 https://doi.org/10.1128/JB.178.3.600-605.1996	journal	January 1996
A Nine-Residue Synthetic Propeptide Enhances Secretion Efficiency of Heterologous Proteins inLactococcus lactis Le Loir, Y.; Gruss, A.; Ehrlich, S. D. Journal of Bacteriology, Vol. 180, Issue 7 https://doi.org/10.1128/JB.180.7.1895-1903.1998	journal	January 1998
Competition and Coexistence between Streptococcus mutans and Streptococcus sanguinis in the Dental Biofilm Kreth, J.; Merritt, J.; Shi, W. Journal of Bacteriology, Vol. 187, Issue 21 https://doi.org/10.1128/JB.187.21.7193-7203.2005	journal	October 2005
Cooperation among Microorganisms Wingreen, Ned S.; Levin, Simon A. PLoS Biology, Vol. 4, Issue 9 https://doi.org/10.1371/journal.pbio.0040299	journal	September 2006
Modifying and reacting to the environmental pH can drive bacterial interactions Ratzke, Christoph; Gore, Jeff PLOS Biology, Vol. 16, Issue 3 https://doi.org/10.1371/journal.pbio.2004248	journal	March 2018
Uncovering and resolving challenges of quantitative modeling in a simplified community of interacting cells Hart, Samuel F. M.; Mi, Hanbing; Green, Robin PLOS Biology, Vol. 17, Issue 2 https://doi.org/10.1371/journal.pbio.3000135	journal	February 2019
Environments that Induce Synthetic Microbial Ecosystems Klitgord, Niels; Segrè, Daniel PLoS Computational Biology, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pcbi.1001002	journal	November 2010
Bistability versus Bimodal Distributions in Gene Regulatory Processes from Population Balance Shu, Che-Chi; Chatterjee, Anushree; Dunny, Gary PLoS Computational Biology, Vol. 7, Issue 8 https://doi.org/10.1371/journal.pcbi.1002140	journal	August 2011
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
Mathematical Modeling of Microbial Community Dynamics: A Methodological Review Song, Hyun-Seob; Cannon, William; Beliaev, Alexander Processes, Vol. 2, Issue 4 https://doi.org/10.3390/pr2040711	journal	October 2014

Similar Records

Dissecting the Division of Labor in Microbial Consortia for the Production of Biofuels and Chemicals (Final Technical Report)

Technical Report · Tue Dec 12 04:00:00 UTC 2023 · OSTI ID:1902819

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Interaction variability shapes succession of synthetic microbial ecosystems

Citation Formats

References (69)

Similar Records

Related Subjects