IDEAS home Printed from https://ideas.repec.org/a/plo/pbio00/3000550.html
   My bibliography  Save this article

High-order interactions distort the functional landscape of microbial consortia

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3000550
    Download Restriction: no

    File URL: https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3000550&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pbio.3000550?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. Karoline Faust & Jeroen Raes, 2016. "Rules of the game for microbiota," Nature, Nature, vol. 534(7606), pages 182-183, June.
    10. 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.
    11. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Gerrit Ansmann & Tobias Bollenbach, 2021. "Building clone-consistent ecosystem models," PLOS Computational Biology, Public Library of Science, vol. 17(2), pages 1-25, February.
    2. Chen, Shiliang & Liu, Xiang & He, Qiang & Zhou, Shurong, 2022. "Higher-order interactions on disease transmission can reverse the dilution effect or weaken the amplification effect to unimodal pattern," Ecological Modelling, Elsevier, vol. 474(C).
    3. Luca Gallo & Lucas Lacasa & Vito Latora & Federico Battiston, 2024. "Higher-order correlations reveal complex memory in temporal hypergraphs," Nature Communications, Nature, vol. 15(1), pages 1-7, December.
    4. Dai, Hui & Wang, Xiaoyue & Lu, Yikang & Hou, Yunxiang & Shi, Lei, 2024. "The effect of intraspecific cooperation in a three-species cyclic predator-prey model," Applied Mathematics and Computation, Elsevier, vol. 470(C).
    5. Rigato, Emanuele & Fusco, Giuseppe, 2020. "A heuristic model of the effects of phenotypic robustness in adaptive evolution," Theoretical Population Biology, Elsevier, vol. 136(C), pages 22-30.
    6. Feng Shi & James Evans, 2023. "Surprising combinations of research contents and contexts are related to impact and emerge with scientific outsiders from distant disciplines," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Miguel A Fortuna & Luis Zaman & Charles Ofria & Andreas Wagner, 2017. "The genotype-phenotype map of an evolving digital organism," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-20, February.
    8. Li, Jie & Shen, Xuzhu & Li, YaoTang, 2021. "Modeling the temporal dynamics of gut microbiota from a local community perspective," Ecological Modelling, Elsevier, vol. 460(C).
    9. Shang, Yilun, 2022. "Sombor index and degree-related properties of simplicial networks," Applied Mathematics and Computation, Elsevier, vol. 419(C).
    10. Papanikolaou, Nikos & Lambiotte, Renaud & Vaccario, Giacomo, 2023. "Fragmentation from group interactions: A higher-order adaptive voter model," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 630(C).
    11. Zhang, Zeyu & Bearup, Daniel & Guo, Guanming & Zhang, Helin & Liao, Jinbao, 2022. "Competition modes determine ecosystem stability in rock–paper–scissors games," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 607(C).
    12. Térence Legrand & Anne Chenuil & Enrico Ser-Giacomi & Sophie Arnaud-Haond & Nicolas Bierne & Vincent Rossi, 2022. "Spatial coalescent connectivity through multi-generation dispersal modelling predicts gene flow across marine phyla," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. David Bruce Borenstein & Yigal Meir & Joshua W Shaevitz & Ned S Wingreen, 2013. "Non-Local Interaction via Diffusible Resource Prevents Coexistence of Cooperators and Cheaters in a Lattice Model," PLOS ONE, Public Library of Science, vol. 8(5), pages 1-10, May.
    14. Jorge Peña & Yannick Rochat, 2012. "Bipartite Graphs as Models of Population Structures in Evolutionary Multiplayer Games," PLOS ONE, Public Library of Science, vol. 7(9), pages 1-13, September.
    15. Xiaojie Chen & Attila Szolnoki, 2018. "Punishment and inspection for governing the commons in a feedback-evolving game," PLOS Computational Biology, Public Library of Science, vol. 14(7), pages 1-15, July.
    16. Brandl, Florian & Brandt, Felix, 2024. "A natural adaptive process for collective decision-making," Theoretical Economics, Econometric Society, vol. 19(2), May.
    17. Sam F Greenbury & Steffen Schaper & Sebastian E Ahnert & Ard A Louis, 2016. "Genetic Correlations Greatly Increase Mutational Robustness and Can Both Reduce and Enhance Evolvability," PLOS Computational Biology, Public Library of Science, vol. 12(3), pages 1-27, March.
    18. Avraham E Mayo & Yaakov Setty & Seagull Shavit & Alon Zaslaver & Uri Alon, 2006. "Plasticity of the cis-Regulatory Input Function of a Gene," PLOS Biology, Public Library of Science, vol. 4(4), pages 1-1, March.
    19. Dongli, Duan & Chengxing, Wu & Yuchen, Zhai & Changchun, Lv & Ning, Wang, 2022. "Coexistence mechanism of alien species and local ecosystem based on network dimensionality reduction method," Chaos, Solitons & Fractals, Elsevier, vol. 159(C).
    20. David García-Callejas & Ignasi Bartomeus & Oscar Godoy, 2021. "The spatial configuration of biotic interactions shapes coexistence-area relationships in an annual plant community," Nature Communications, Nature, vol. 12(1), pages 1-8, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pbio00:3000550. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosbiology (email available below). General contact details of provider: https://journals.plos.org/plosbiology/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.