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High-order interactions distort the functional landscape of microbial consortia

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  • Alicia Sanchez-Gorostiaga
  • Djordje Bajić
  • Melisa L Osborne
  • Juan F Poyatos
  • Alvaro Sanchez

Abstract

Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantitatively predicted from traits of species in monoculture. Inspired by the study of complex genetic interactions, we have examined how the amylolytic rate of combinatorial assemblages of six starch-degrading soil bacteria depend on the separate functional contributions from each species and their interactions. Filtering our results through the theory of biochemical kinetics, we show that this simple function is additive in the absence of interactions among community members. For about half of the combinatorially assembled consortia, the amylolytic function is dominated by pairwise and higher-order interactions. For the other half, the function is additive despite the presence of strong competitive interactions. We explain the mechanistic basis of these findings and propose a quantitative framework that allows us to separate the effect of behavioral and population dynamics interactions. Our results suggest that the functional robustness of a consortium to pairwise and higher-order interactions critically affects our ability to predict and bottom-up engineer ecosystem function in complex communities.Can we predict the function of a microbial consortium? This study shows that even a simple function can exhibit substantial complexity and be dominated by complex interactions, illustrating the important challenges that arise when trying to design synthetic microbial consortia from first principles.

Suggested Citation

  • Alicia Sanchez-Gorostiaga & Djordje Bajić & Melisa L Osborne & Juan F Poyatos & Alvaro Sanchez, 2019. "High-order interactions distort the functional landscape of microbial consortia," PLOS Biology, Public Library of Science, vol. 17(12), pages 1-34, December.
  • Handle: RePEc:plo:pbio00:3000550
    DOI: 10.1371/journal.pbio.3000550
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    References listed on IDEAS

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    1. Jacopo Grilli & György Barabás & Matthew J. Michalska-Smith & Stefano Allesina, 2017. "Higher-order interactions stabilize dynamics in competitive network models," Nature, Nature, vol. 548(7666), pages 210-213, August.
    2. Xiaokan Guo & James Q Boedicker, 2016. "The Contribution of High-Order Metabolic Interactions to the Global Activity of a Four-Species Microbial Community," PLOS Computational Biology, Public Library of Science, vol. 12(9), pages 1-13, September.
    3. Jeremy A. Draghi & Todd L. Parsons & Günter P. Wagner & Joshua B. Plotkin, 2010. "Mutational robustness can facilitate adaptation," Nature, Nature, vol. 463(7279), pages 353-355, January.
    4. Karen S. Sarkisyan & Dmitry A. Bolotin & Margarita V. Meer & Dinara R. Usmanova & Alexander S. Mishin & George V. Sharonov & Dmitry N. Ivankov & Nina G. Bozhanova & Mikhail S. Baranov & Onuralp Soylem, 2016. "Local fitness landscape of the green fluorescent protein," Nature, Nature, vol. 533(7603), pages 397-401, May.
    5. Aditya Barve & Andreas Wagner, 2013. "A latent capacity for evolutionary innovation through exaptation in metabolic systems," Nature, Nature, vol. 500(7461), pages 203-206, August.
    6. Jeff Gore & Hyun Youk & Alexander van Oudenaarden, 2009. "Snowdrift game dynamics and facultative cheating in yeast," Nature, Nature, vol. 459(7244), pages 253-256, May.
    7. Jonathan M. Levine & Jordi Bascompte & Peter B. Adler & Stefano Allesina, 2017. "Beyond pairwise mechanisms of species coexistence in complex communities," Nature, Nature, vol. 546(7656), pages 56-64, June.
    8. Eyal Bairey & Eric D. Kelsic & Roy Kishony, 2016. "High-order species interactions shape ecosystem diversity," Nature Communications, Nature, vol. 7(1), pages 1-7, November.
    9. Timothy S. Gardner & Charles R. Cantor & James J. Collins, 2000. "Construction of a genetic toggle switch in Escherichia coli," Nature, Nature, vol. 403(6767), pages 339-342, January.
    10. Karoline Faust & Jeroen Raes, 2016. "Rules of the game for microbiota," Nature, Nature, vol. 534(7606), pages 182-183, June.
    11. Frank J. Poelwijk & Daniel J. Kiviet & Daniel M. Weinreich & Sander J. Tans, 2007. "Empirical fitness landscapes reveal accessible evolutionary paths," Nature, Nature, vol. 445(7126), pages 383-386, January.
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    Cited by:

    1. Lu Wu & Xu-Wen Wang & Zining Tao & Tong Wang & Wenlong Zuo & Yu Zeng & Yang-Yu Liu & Lei Dai, 2024. "Data-driven prediction of colonization outcomes for complex microbial communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Guy Amit & Amir Bashan, 2023. "Top-down identification of keystone taxa in the microbiome," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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