Environmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communities
Abstract
Phototrophic communities of photosynthetic algae or cyanobacteria and heterotrophic bacteria or fungi are pervasive throughout the environment. How interactions between members contribute to the resilience and affect the fitness of phototrophic communities is not fully understood. In this work, we integrated metatranscriptomics, metabolomics and phenotyping with computational modelling to reveal condition-dependent secretion and cross-feeding of metabolites in a synthetic community. We discovered that interactions between members are highly dynamic and are driven by the availability of organic and inorganic nutrients. Environmental factors, such as ammonia concentration, influenced community stability by shifting members from collaborating to competing. Moreover, overall fitness was dependent on genotype and streamlined genomes improved growth of the entire community. Our mechanistic framework offers insights into the physiology and metabolic response to environmental and genetic perturbation of these ubiquitous microbial associations.
- Authors:
-
[1];
[2];
[1]
- Univ. of California, San Diego, CA (United States)
- Johns Hopkins Univ., Baltimore, MD (United States)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1571390
- Report Number(s):
- NREL/JA-5100-74455
Journal ID: ISSN 2058-5276
- Grant/Contract Number:
- AC36-08GO28308
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Microbiology
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 12; Journal ID: ISSN 2058-5276
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; bioenergy; industrial biotechnology
Citation Formats
Zuñiga, Cristal, Li, Chien-Ting, Yu, Geng, Al-Bassam, Mahmoud M., Li, Tingting, Jiang, Liqun, Zaramela, Livia S., Guarnieri, Michael, Betenbaugh, Michael J., and Zengler, Karsten. Environmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communities. United States: N. p., 2019.
Web. doi:10.1038/s41564-019-0567-6.
Zuñiga, Cristal, Li, Chien-Ting, Yu, Geng, Al-Bassam, Mahmoud M., Li, Tingting, Jiang, Liqun, Zaramela, Livia S., Guarnieri, Michael, Betenbaugh, Michael J., & Zengler, Karsten. Environmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communities. United States. https://doi.org/10.1038/s41564-019-0567-6
Zuñiga, Cristal, Li, Chien-Ting, Yu, Geng, Al-Bassam, Mahmoud M., Li, Tingting, Jiang, Liqun, Zaramela, Livia S., Guarnieri, Michael, Betenbaugh, Michael J., and Zengler, Karsten. Mon .
"Environmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communities". United States. https://doi.org/10.1038/s41564-019-0567-6. https://www.osti.gov/servlets/purl/1571390.
@article{osti_1571390,
title = {Environmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communities},
author = {Zuñiga, Cristal and Li, Chien-Ting and Yu, Geng and Al-Bassam, Mahmoud M. and Li, Tingting and Jiang, Liqun and Zaramela, Livia S. and Guarnieri, Michael and Betenbaugh, Michael J. and Zengler, Karsten},
abstractNote = {Phototrophic communities of photosynthetic algae or cyanobacteria and heterotrophic bacteria or fungi are pervasive throughout the environment. How interactions between members contribute to the resilience and affect the fitness of phototrophic communities is not fully understood. In this work, we integrated metatranscriptomics, metabolomics and phenotyping with computational modelling to reveal condition-dependent secretion and cross-feeding of metabolites in a synthetic community. We discovered that interactions between members are highly dynamic and are driven by the availability of organic and inorganic nutrients. Environmental factors, such as ammonia concentration, influenced community stability by shifting members from collaborating to competing. Moreover, overall fitness was dependent on genotype and streamlined genomes improved growth of the entire community. Our mechanistic framework offers insights into the physiology and metabolic response to environmental and genetic perturbation of these ubiquitous microbial associations.},
doi = {10.1038/s41564-019-0567-6},
journal = {Nature Microbiology},
number = 12,
volume = 4,
place = {United States},
year = {2019},
month = {10}
}
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Works referenced in this record:
Evolutionary limits to cooperation in microbial communities
journal, December 2014
- Oliveira, Nuno M.; Niehus, Rene; Foster, Kevin R.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 50
Physiological Status and Community Composition of Microbial Mats of the Ebro Delta, Spain, by Signature Lipid Biomarkers
journal, January 2000
- Navarrete, A.; Peacock, A.; Macnaughton, S. J.
- Microbial Ecology, Vol. 39, Issue 1
The dynamics of molecular evolution over 60,000 generations
journal, October 2017
- Good, Benjamin H.; McDonald, Michael J.; Barrick, Jeffrey E.
- Nature, Vol. 551, Issue 7678
Species-specific structural and functional diversity of bacterial communities in lichen symbioses
journal, June 2009
- Grube, Martin; Cardinale, Massimiliano; de Castro, João Vieira
- The ISME Journal, Vol. 3, Issue 9
Symbiosis constraints: Strong mycobiont control limits nutrient response in lichens
journal, August 2017
- Palmqvist, Kristin; Franklin, Oskar; Näsholm, Torgny
- Ecology and Evolution, Vol. 7, Issue 18
Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective
journal, September 2003
- Wink, Michael
- Phytochemistry, Vol. 64, Issue 1
Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform
journal, March 2017
- Li, Tingting; Li, Chien-Ting; Butler, Kirk
- Biotechnology for Biofuels, Vol. 10, Issue 1
Environments that Induce Synthetic Microbial Ecosystems
journal, November 2010
- Klitgord, Niels; Segrè, Daniel
- PLoS Computational Biology, Vol. 6, Issue 11
Elucidation of complexity and prediction of interactions in microbial communities
journal, August 2017
- Zuñiga, Cristal; Zaramela, Livia; Zengler, Karsten
- Microbial Biotechnology, Vol. 10, Issue 6
Connecting extracellular metabolomic measurements to intracellular flux states in yeast
journal, January 2009
- Mo, Monica L.; Palsson, Bernhard Ø; Herrgård, Markus J.
- BMC Systems Biology, Vol. 3, Issue 1
The Growth of Lichens With Special Reference to the Modelling of Circular Thalli
journal, October 1981
- Hill, D. J.
- The Lichenologist, Vol. 13, Issue 3
Overflow metabolism in Escherichia coli results from efficient proteome allocation
journal, December 2015
- Basan, Markus; Hui, Sheng; Okano, Hiroyuki
- Nature, Vol. 528, Issue 7580
Bacteria and archaea on Earth and their abundance in biofilms
journal, February 2019
- Flemming, Hans-Curt; Wuertz, Stefan
- Nature Reviews Microbiology, Vol. 17, Issue 4
Niche engineering demonstrates a latent capacity for fungal-algal mutualism
journal, July 2014
- Hom, Erik F. Y.; Murray, Andrew W.
- Science, Vol. 345, Issue 6192
The evolution of cooperation within the gut microbiota
journal, April 2016
- Rakoff-Nahoum, Seth; Foster, Kevin R.; Comstock, Laurie E.
- Nature, Vol. 533, Issue 7602
Nonlinear partial differential equations and applications: Cultivating the uncultured
journal, November 2002
- Zengler, K.; Toledo, G.; Rappe, M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 24
Streamlining and Simplification of Microbial Genome Architecture
journal, October 2006
- Lynch, Michael
- Annual Review of Microbiology, Vol. 60, Issue 1
Comparison of the predicted and observed secondary structure of T4 phage lysozyme
journal, October 1975
- Matthews, B. W.
- Biochimica et Biophysica Acta (BBA) - Protein Structure, Vol. 405, Issue 2
Database resources of the National Center for Biotechnology Information
journal, November 2017
- Agarwala, Richa; Barrett, Tanya; Beck, Jeff
- Nucleic Acids Research, Vol. 46, Issue D1
The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
journal, March 2012
- Morris, J. Jeffrey; Lenski, Richard E.; Zinser, Erik R.
- mBio, Vol. 3, Issue 2
Thermodynamic favorability and pathway yield as evolutionary tradeoffs in biosynthetic pathway choice
journal, October 2018
- Du, Bin; Zielinski, Daniel C.; Monk, Jonathan M.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 44
The social network of microorganisms — how auxotrophies shape complex communities
journal, March 2018
- Zengler, Karsten; Zaramela, Livia S.
- Nature Reviews Microbiology, Vol. 16, Issue 6
Indirect effects drive coevolution in mutualistic networks
journal, October 2017
- Guimarães, Paulo R.; Pires, Mathias M.; Jordano, Pedro
- Nature, Vol. 550, Issue 7677
Predicting Dynamic Metabolic Demands in the Photosynthetic Eukaryote Chlorella vulgaris
journal, September 2017
- Zuñiga, Cristal; Levering, Jennifer; Antoniewicz, Maciek R.
- Plant Physiology, Vol. 176, Issue 1
A road map for the development of community systems (CoSy) biology
journal, March 2012
- Zengler, Karsten; Palsson, Bernhard O.
- Nature Reviews Microbiology, Vol. 10, Issue 5
EcoFABs: advancing microbiome science through standardized fabricated ecosystems
journal, June 2019
- Zengler, Karsten; Hofmockel, Kirsten; Baliga, Nitin S.
- Nature Methods, Vol. 16, Issue 7
Interactions between Diatoms and Bacteria
journal, August 2012
- Amin, S. A.; Parker, M. S.; Armbrust, E. V.
- Microbiology and Molecular Biology Reviews, Vol. 76, Issue 3
Survival Potential and Photosynthetic Activity of Lichens Under Mars-Like Conditions: A Laboratory Study
journal, March 2010
- Vera, Jean-Pierre de; Möhlmann, Diedrich; Butina, Frederike
- Astrobiology, Vol. 10, Issue 2
Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0
journal, August 2011
- Schellenberger, Jan; Que, Richard; Fleming, Ronan M. T.
- Nature Protocols, Vol. 6, Issue 9
The Chlorella vulgaris S-Nitrosoproteome under Nitrogen-Replete and -Deplete Conditions
journal, January 2017
- Henard, Calvin A.; Guarnieri, Michael T.; Knoshaug, Eric P.
- Frontiers in Bioengineering and Biotechnology, Vol. 4
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013
- Liao, Y.; Smyth, G. K.; Shi, W.
- Bioinformatics, Vol. 30, Issue 7
Characterization and modelling of interspecies electron transfer mechanisms and microbial community dynamics of a syntrophic association
journal, November 2013
- Nagarajan, Harish; Embree, Mallory; Rotaru, Amelia-Elena
- Nature Communications, Vol. 4, Issue 1
Flux Imbalance Analysis and the Sensitivity of Cellular Growth to Changes in Metabolite Pools
journal, August 2013
- Reznik, Ed; Mehta, Pankaj; Segrè, Daniel
- PLoS Computational Biology, Vol. 9, Issue 8
Microbial mat ecosystems: Structure types, functional diversity, and biotechnological application
journal, January 2018
- Prieto-Barajas, Cristina M.; Valencia-Cantero, Eduardo; Santoyo, Gustavo
- Electronic Journal of Biotechnology, Vol. 31
A functional perspective on phenotypic heterogeneity in microorganisms
journal, July 2015
- Ackermann, Martin
- Nature Reviews Microbiology, Vol. 13, Issue 8
Lichen symbiosis: Search and recognition of partners
journal, September 2016
- Insarova, I. D.; Blagoveshchenskaya, E. Yu.
- Biology Bulletin, Vol. 43, Issue 5
A comprehensive strategy enabling high-resolution functional analysis of the yeast genome
journal, July 2008
- Breslow, David K.; Cameron, Dale M.; Collins, Sean R.
- Nature Methods, Vol. 5, Issue 8
Eutrophic lichens respond to multiple forms of N: implications for critical levels and critical loads research
journal, October 2012
- Jovan, Sarah; Riddell, Jennifer; Padgett, Pamela E.
- Ecological Applications, Vol. 22, Issue 7
Predicting proteome allocation, overflow metabolism, and metal requirements in a model acetogen
journal, March 2019
- Liu, Joanne K.; Lloyd, Colton; Al-Bassam, Mahmoud M.
- PLOS Computational Biology, Vol. 15, Issue 3
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Genome-Scale Metabolic Model for the Green Alga Chlorella vulgaris UTEX 395 Accurately Predicts Phenotypes under Autotrophic, Heterotrophic, and Mixotrophic Growth Conditions
journal, July 2016
- Zuñiga, Cristal; Li, Chien-Ting; Huelsman, Tyler
- Plant Physiology, Vol. 172, Issue 1
Leucine incorporation by aerobic anoxygenic phototrophic bacteria in the Delaware estuary
journal, May 2014
- Stegman, Monica R.; Cottrell, Matthew T.; Kirchman, David L.
- The ISME Journal, Vol. 8, Issue 11
Need for Laboratory Ecosystems To Unravel the Structures and Functions of Soil Microbial Communities Mediated by Chemistry
journal, July 2018
- Zhalnina, Kateryna; Zengler, Karsten; Newman, Dianne
- mBio, Vol. 9, Issue 4
Carbon and nitrogen distribution in the green algal lichens Hypogymnia physodes and Platismatia glauca in relation to nutrient supply
journal, January 2003
- Dahlman, Lena; Persson, Jörgen; Näsholm, Torgny
- Planta, Vol. 217, Issue 1
Influence of Mycosphaerella and Teratosphaeria leaf diseases on chemical composition of essential oils of Eucalyptus globulus and effect of these essential oils on ascospores germination
journal, April 2021
- Passador, Martha Maria; Marubayashi, Julio Massaharu; Uzzo, Roberta Pierry
- Archives of Microbiology, Vol. 203, Issue 6
Database resources of the National Center for Biotechnology Information
journal, January 2006
- Wheeler, D. L.
- Nucleic Acids Research, Vol. 34, Issue 90001
Indirect effects drive coevolution in mutualistic networks
text, January 2017
- Guimarães, Paulo R.; Pires, Mathias M.; Jordano, Pedro
- Nature Publishing Group
Activity landscape image analysis using convolutional neural networks
text, January 2020
- Iqbal, Javed; Vogt, Martin; Bajorath, Jürgen
- Zenodo
Database resources of the National Center for Biotechnology Information
journal, October 2020
- Sayers, Eric W.; Beck, Jeffrey; Bolton, Evan E.
- Nucleic Acids Research, Vol. 49, Issue D1
Database resources of the National Center for Biotechnology Information
journal, December 2007
- Wheeler, D. L.; Barrett, T.; Benson, D. A.
- Nucleic Acids Research, Vol. 36, Issue Database
Database resources of the National Center for Biotechnology Information
journal, November 2018
- Sayers, Eric W.; Agarwala, Richa; Bolton, Evan E.
- Nucleic Acids Research, Vol. 47, Issue D1
featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features
text, January 2013
- Liao, Yang; Smyth, Gordon K.; Shi, Wei
- arXiv