Environmental fluctuations reshape an unexpected diversity-disturbance relationship in a microbial community

  1. Christopher P Mancuso
  2. Hyunseok Lee
  3. Clare I Abreu
  4. Jeff Gore
  5. Ahmad S Khalil  Is a corresponding author
  1. Boston University, United States
  2. Massachusetts Institute of Technology, United States

Abstract

Environmental disturbances have long been theorized to play a significant role in shaping the diversity and composition of ecosystems. However, an inability to specify the characteristics of a disturbance experimentally has produced an inconsistent picture of diversity-disturbance relationships (DDRs). Here, using a high-throughput programmable culture system, we subjected a soil-derived bacterial community to dilution disturbance profiles with different intensities (mean dilution rates), applied either constantly or with fluctuations of different frequencies. We observed an unexpected U-shaped relationship between community diversity and disturbance intensity in the absence of fluctuations. Adding fluctuations increased community diversity and erased the U-shape. All our results are well-captured by a Monod consumer resource model, which also explains how U-shaped DDRs emerge via a novel 'niche flip' mechanism. Broadly, our combined experimental and modeling framework demonstrates how distinct features of an environmental disturbance can interact in complex ways to govern ecosystem assembly and offers strategies for reshaping the composition of microbiomes.

Data availability

All sequencing data is deposited in the Sequence Read Archive (SRA) accessible with a BioProject accession code PRJNA719465. Agar plate images are deposited on Figshare accessible at doi.org/10.6084/m9.figshare.15117558. Computer code used to run eVOLVER experiments and for theoretical modeling is available at github.com/khalillab. All other datasets required to produce the results in the current study are included as supplemental data. Source data files have been provided.

The following data sets were generated

Article and author information

Author details

  1. Christopher P Mancuso

    Biomedical Engineering, Boston University, Boston, United States
    Competing interests
    No competing interests declared.
  2. Hyunseok Lee

    Physics, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1554-6228
  3. Clare I Abreu

    Physics, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    No competing interests declared.
  4. Jeff Gore

    Physics of Living Systems, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4583-8555
  5. Ahmad S Khalil

    Department of Biomedical Engineering, Boston University, Boston, United States
    For correspondence
    khalil@bu.edu
    Competing interests
    Ahmad S Khalil, A.S.K. is co-founder of Fynch Biosciences, a manufacturer of eVOLVER hardware..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8214-0546

Funding

Defense Advanced Research Projects Agency (HR001115C0091)

  • Ahmad S Khalil

Defense Advanced Research Projects Agency (HR001117S0029)

  • Ahmad S Khalil

Simons Foundation (542385)

  • Jeff Gore

National Institute of General Medical Sciences (R01GM102311)

  • Jeff Gore

National Institute of Biomedical Imaging and Bioengineering (R01EB027793)

  • Ahmad S Khalil

National Institutes of Health (DP2AI131083)

  • Ahmad S Khalil

National Science Foundation (MCB-1350949)

  • Ahmad S Khalil

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Wenying Shou, University College London, United Kingdom

Version history

  1. Preprint posted: July 29, 2020 (view preprint)
  2. Received: February 2, 2021
  3. Accepted: August 27, 2021
  4. Accepted Manuscript published: September 3, 2021 (version 1)
  5. Version of Record published: September 23, 2021 (version 2)

Copyright

© 2021, Mancuso et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Christopher P Mancuso
  2. Hyunseok Lee
  3. Clare I Abreu
  4. Jeff Gore
  5. Ahmad S Khalil
(2021)
Environmental fluctuations reshape an unexpected diversity-disturbance relationship in a microbial community
eLife 10:e67175.
https://doi.org/10.7554/eLife.67175

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https://doi.org/10.7554/eLife.67175

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