Alternative stable states, nonlinear behavior, and predictability of microbiome dynamics

Hiroaki Fujita*, Masayuki Ushio, Kenta Suzuki, Masato S. Abe, Masato Yamamichi, Koji Iwayama, Alberto Canarini, Ibuki Hayashi, Keitaro Fukushima, Shinji Fukuda, E. Toby Kiers, Hirokazu Toju*

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Background: Microbiome dynamics are both crucial indicators and potential drivers of human health, agricultural output, and industrial bio-applications. However, predicting microbiome dynamics is notoriously difficult because communities often show abrupt structural changes, such as “dysbiosis” in human microbiomes. Methods: We integrated theoretical frameworks and empirical analyses with the aim of anticipating drastic shifts of microbial communities. We monitored 48 experimental microbiomes for 110 days and observed that various community-level events, including collapse and gradual compositional changes, occurred according to a defined set of environmental conditions. We analyzed the time-series data based on statistical physics and non-linear mechanics to describe the characteristics of the microbiome dynamics and to examine the predictability of major shifts in microbial community structure. Results: We confirmed that the abrupt community changes observed through the time-series could be described as shifts between “alternative stable states“ or dynamics around complex attractors. Furthermore, collapses of microbiome structure were successfully anticipated by means of the diagnostic threshold defined with the “energy landscape” analysis of statistical physics or that of a stability index of nonlinear mechanics. Conclusions: The results indicate that abrupt microbiome events in complex microbial communities can be forecasted by extending classic ecological concepts to the scale of species-rich microbial systems. [MediaObject not available: see fulltext.].

Original languageEnglish
Article number63
Pages (from-to)1-16
Number of pages16
JournalMicrobiome
Volume11
DOIs
Publication statusPublished - 29 Mar 2023

Bibliographical note

Funding Information:
This work was financially supported by JST PRESTO (JPMJPR16Q6), Human Frontier Science Program (RGP0029/2019), JSPS Grant-in-Aid for Scientific Research (20K20586), NEDO Moonshot Research and Development Program (JPNP18016), and JST FOREST (JPMJFR2048) to H.T., JSPS Grant-in-Aid for Scientific Research (20K06820 and 20H03010) to K.S., and JSPS Fellowship to H.F. and A.C.

Funding Information:
We thank Sayaka Suzuki and Keisuke Koba for support in the experiment and Tadashi Fukami and anonymous reviewers for insightful comments on the manuscript. Computation time was provided by the SuperComputer System, Institute for Chemical Research, Kyoto University.

Publisher Copyright:
© 2023, The Author(s).

Funding

This work was financially supported by JST PRESTO (JPMJPR16Q6), Human Frontier Science Program (RGP0029/2019), JSPS Grant-in-Aid for Scientific Research (20K20586), NEDO Moonshot Research and Development Program (JPNP18016), and JST FOREST (JPMJFR2048) to H.T., JSPS Grant-in-Aid for Scientific Research (20K06820 and 20H03010) to K.S., and JSPS Fellowship to H.F. and A.C. We thank Sayaka Suzuki and Keisuke Koba for support in the experiment and Tadashi Fukami and anonymous reviewers for insightful comments on the manuscript. Computation time was provided by the SuperComputer System, Institute for Chemical Research, Kyoto University.

FundersFunder number
Sayaka Suzuki and Keisuke Koba
Tadashi Fukami
Human Frontier Science ProgramRGP0029/2019
Japan Society for the Promotion of Science20K20586, 22H02688
Precursory Research for Embryonic Science and TechnologyJPMJPR16Q6
JST FORESTJPMJFR2048, 20K06820, 20H03010
Moonshot Research and Development ProgramJPNP18016

    Keywords

    • Alternative stable states
    • Biodiversity
    • Biological communities
    • Chaos
    • Community collapse
    • Community stability
    • Dysbiosis
    • Empirical dynamic modeling
    • Microbiome dynamics
    • Non-linear dynamics

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