DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Integrating ecological and engineering concepts of resilience in microbial communities

Abstract

We note that many definitions of resilience have been proffered for natural and engineered ecosystems, but a conceptual consensus on resilience in microbial communities is still lacking. Here, we argue that the disconnect largely results from the wide variance in microbial community complexity, which range from simple synthetic consortia to complex natural communities, and divergence between the typical practical outcomes emphasized by ecologists and engineers. Viewing microbial communities as elasto-plastic systems, we argue that this gap between the engineering and ecological definitions of resilience stems from their respective emphases on elastic and plastic deformation, respectively. We propose that the two concepts may be fundamentally united around the resilience of function rather than state in microbial communities and the regularity in the relationship between environmental variation and a community’s functional response. Furthermore, we posit that functional resilience is an intrinsic property of microbial communities, suggesting that state changes in response to environmental variation may be a key mechanism driving resilience in microbial communities.

Authors:
 [1];  [2];  [1];  [1]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1240232
Report Number(s):
PNNL-SA-112189
Journal ID: ISSN 1664-302X; KP1601010
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; microbial communities; microbial ecology; resilience; resistance; robustness; stability; networks

Citation Formats

Song, Hyun -Seob, Renslow, Ryan S., Fredrickson, Jim K., and Lindemann, Stephen R. Integrating ecological and engineering concepts of resilience in microbial communities. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.01298.
Song, Hyun -Seob, Renslow, Ryan S., Fredrickson, Jim K., & Lindemann, Stephen R. Integrating ecological and engineering concepts of resilience in microbial communities. United States. https://doi.org/10.3389/fmicb.2015.01298
Song, Hyun -Seob, Renslow, Ryan S., Fredrickson, Jim K., and Lindemann, Stephen R. Tue . "Integrating ecological and engineering concepts of resilience in microbial communities". United States. https://doi.org/10.3389/fmicb.2015.01298. https://www.osti.gov/servlets/purl/1240232.
@article{osti_1240232,
title = {Integrating ecological and engineering concepts of resilience in microbial communities},
author = {Song, Hyun -Seob and Renslow, Ryan S. and Fredrickson, Jim K. and Lindemann, Stephen R.},
abstractNote = {We note that many definitions of resilience have been proffered for natural and engineered ecosystems, but a conceptual consensus on resilience in microbial communities is still lacking. Here, we argue that the disconnect largely results from the wide variance in microbial community complexity, which range from simple synthetic consortia to complex natural communities, and divergence between the typical practical outcomes emphasized by ecologists and engineers. Viewing microbial communities as elasto-plastic systems, we argue that this gap between the engineering and ecological definitions of resilience stems from their respective emphases on elastic and plastic deformation, respectively. We propose that the two concepts may be fundamentally united around the resilience of function rather than state in microbial communities and the regularity in the relationship between environmental variation and a community’s functional response. Furthermore, we posit that functional resilience is an intrinsic property of microbial communities, suggesting that state changes in response to environmental variation may be a key mechanism driving resilience in microbial communities.},
doi = {10.3389/fmicb.2015.01298},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Tue Dec 01 00:00:00 EST 2015},
month = {Tue Dec 01 00:00:00 EST 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 38 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Lake microbial communities are resilient after a whole-ecosystem disturbance
journal, June 2012

  • Shade, Ashley; Read, Jordan S.; Youngblut, Nicholas D.
  • The ISME Journal, Vol. 6, Issue 12
  • DOI: 10.1038/ismej.2012.56

Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest
journal, April 2014

  • Taş, Neslihan; Prestat, Emmanuel; McFarland, Jack W.
  • The ISME Journal, Vol. 8, Issue 9
  • DOI: 10.1038/ismej.2014.36

Prokaryotes: The unseen majority
journal, June 1998

  • Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
  • DOI: 10.1073/pnas.95.12.6578

Slow Recovery from Perturbations as a Generic Indicator of a Nearby Catastrophic Shift
journal, June 2007

  • van Nes, Egbert H.; Scheffer, Marten
  • The American Naturalist, Vol. 169, Issue 6
  • DOI: 10.1086/516845

Erratum: Corrigendum: Recovery rates reflect distance to a tipping point in a living system
journal, April 2012

  • Veraart, Annelies J.; Faassen, Elisabeth J.; Dakos, Vasilis
  • Nature, Vol. 484, Issue 7394
  • DOI: 10.1038/nature11029

What is microbial community ecology?
journal, August 2009


Ecological control analysis: being(s) in control of mass flux and metabolite concentrations in anaerobic degradation processes
journal, February 2007


Fundamentals of Microbial Community Resistance and Resilience
journal, January 2012


Networked buffering: a basic mechanism for distributed robustness in complex adaptive systems
journal, June 2010

  • Whitacre, James M.; Bender, Axel
  • Theoretical Biology and Medical Modelling, Vol. 7, Issue 1
  • DOI: 10.1186/1742-4682-7-20

Marine microbial community dynamics and their ecological interpretation
journal, February 2015

  • Fuhrman, Jed A.; Cram, Jacob A.; Needham, David M.
  • Nature Reviews Microbiology, Vol. 13, Issue 3
  • DOI: 10.1038/nrmicro3417

Mathematical Modeling of Microbial Community Dynamics: A Methodological Review
journal, October 2014

  • Song, Hyun-Seob; Cannon, William; Beliaev, Alexander
  • Processes, Vol. 2, Issue 4
  • DOI: 10.3390/pr2040711

Resistance, resilience, and redundancy in microbial communities
journal, August 2008

  • Allison, S. D.; Martiny, J. B. H.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1
  • DOI: 10.1073/pnas.0801925105

Complex Nonlinear Behavior in Metabolic Processes: Global Bifurcation Analysis of Escherichia coli Growth on Multiple Substrates
journal, September 2013

  • Song, Hyun-Seob; Ramkrishna, Doraiswami
  • Processes, Vol. 1, Issue 3
  • DOI: 10.3390/pr1030263

Microbiome Data Distinguish Patients with Clostridium difficile Infection and Non-C. difficile-Associated Diarrhea from Healthy Controls
journal, May 2014

  • Schubert, Alyxandria M.; Rogers, Mary A. M.; Ring, Cathrin
  • mBio, Vol. 5, Issue 3
  • DOI: 10.1128/mbio.01021-14

Predicting a Human Gut Microbiota's Response to Diet in Gnotobiotic Mice
journal, May 2011


Rising to the challenge of sustaining coral reef resilience
journal, November 2010

  • Hughes, Terry P.; Graham, Nicholas A. J.; Jackson, Jeremy B. C.
  • Trends in Ecology & Evolution, Vol. 25, Issue 11
  • DOI: 10.1016/j.tree.2010.07.011

Generic Indicators for Loss of Resilience Before a Tipping Point Leading to Population Collapse
journal, May 2012


Microbiota Dynamics in Patients Treated with Fecal Microbiota Transplantation for Recurrent Clostridium difficile Infection
journal, November 2013


Wastewater treatment high rate algal ponds for biofuel production
journal, January 2011


Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection
journal, March 2015


Critical slowing down as early warning for the onset of collapse in mutualistic communities
journal, November 2014

  • Dakos, Vasilis; Bascompte, Jordi
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 49
  • DOI: 10.1073/pnas.1406326111

Resilience and Stability of Ecological Systems
journal, November 1973


The epsomitic phototrophic microbial mat of Hot Lake, Washington: community structural responses to seasonal cycling
journal, January 2013

  • Lindemann, Stephen R.; Moran, James J.; Stegen, James C.
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00323

Microbial Ecology of Ocean Biogeochemistry: A Community Perspective
journal, May 2008


Biological robustness
journal, November 2004

  • Kitano, Hiroaki
  • Nature Reviews Genetics, Vol. 5, Issue 11
  • DOI: 10.1038/nrg1471

Effects of Biodiversity on Ecosystem Functioning: a Consensus of Current Knowledge
journal, February 2005

  • Hooper, D. U.; Chapin, F. S.; Ewel, J. J.
  • Ecological Monographs, Vol. 75, Issue 1
  • DOI: 10.1890/04-0922

Dynamics in microbial communities: unraveling mechanisms to identify principles
journal, December 2014

  • Konopka, Allan; Lindemann, Stephen; Fredrickson, Jim
  • The ISME Journal, Vol. 9, Issue 7
  • DOI: 10.1038/ismej.2014.251

Multiple High-Throughput Analyses Monitor the Response of E. coli to Perturbations
journal, April 2007


Reverse Engineering of Biological Complexity
journal, March 2002


Long-term monitoring reveals stable and remarkably similar microbial communities in parallel full-scale biogas reactors digesting energy crops
journal, January 2015

  • Lucas, Rico; Kuchenbuch, Anne; Fetzer, Ingo
  • FEMS Microbiology Ecology, Vol. 91, Issue 3
  • DOI: 10.1093/femsec/fiv004

Individualized medicine and the microbiome in reproductive tract
journal, April 2015

  • Braundmeier, Andrea G.; Lenz, Katherine M.; Inman, Kristin S.
  • Frontiers in Physiology, Vol. 6
  • DOI: 10.3389/fphys.2015.00097

What Is Resilience? A Short Introduction
book, January 2011


From Metaphor to Measurement: Resilience of What to What?
journal, December 2001


Global Resilience of Tropical Forest and Savanna to Critical Transitions
journal, October 2011


Exacting predictions by cybernetic model confirmed experimentally: Steady state multiplicity in the chemostat
journal, July 2012

  • Kim, Jin Il; Song, Hyun-Seob; Sunkara, Sunil R.
  • Biotechnology Progress, Vol. 28, Issue 5
  • DOI: 10.1002/btpr.1583

Prediction of Metabolic Flux Distribution from Gene Expression Data Based on the Flux Minimization Principle
journal, November 2014


Slower recovery in space before collapse of connected populations
journal, April 2013

  • Dai, Lei; Korolev, Kirill S.; Gore, Jeff
  • Nature, Vol. 496, Issue 7445
  • DOI: 10.1038/nature12071

Invariability of central metabolic flux distribution in Shewanella oneidensis MR-1 under environmental or genetic perturbations
journal, July 2009

  • Tang, Yinjie J.; Martin, Hector Garcia; Deutschbauer, Adam
  • Biotechnology Progress, Vol. 25, Issue 5
  • DOI: 10.1002/btpr.227

Highly optimized tolerance: A mechanism for power laws in designed systems
journal, August 1999


Insights into the resistance and resilience of the soil microbial community
journal, March 2013


The Microbial Engines That Drive Earth's Biogeochemical Cycles
journal, May 2008


No Vacancy: How Beneficial Microbes Cooperate with Immunity To Provide Colonization Resistance to Pathogens
journal, April 2015

  • Sassone-Corsi, Martina; Raffatellu, Manuela
  • The Journal of Immunology, Vol. 194, Issue 9
  • DOI: 10.4049/jimmunol.1403169

Resilience, Robustness, and Marine Ecosystem-based Management
journal, January 2008

  • Levin, Simon A.; Lubchenco, Jane
  • BioScience, Vol. 58, Issue 1
  • DOI: 10.1641/B580107

Staphylococcus aureus Induces Hypoxia and Cellular Damage in Porcine Dermal Explants
journal, April 2015

  • Lone, Abdul G.; Atci, Erhan; Renslow, Ryan
  • Infection and Immunity, Vol. 83, Issue 6
  • DOI: 10.1128/IAI.03075-14

Evidence of Microbial Regulation of Biogeochemical Cycles from a Study on Methane Flux and Land Use Change
journal, April 2013

  • Nazaries, Loïc; Pan, Yao; Bodrossy, Levente
  • Applied and Environmental Microbiology, Vol. 79, Issue 13
  • DOI: 10.1128/AEM.00095-13

Generic Indicators for Loss of Resilience Before a Tipping Point Leading to Population Collapse
journal, March 2013


Biological Robustness
text, January 2018


Effects of biodiversity on ecosystem functioning: a consensus of current knowledge
text, January 2005

  • Hooper, D. U.; S., Chapin III, F.; Ewel, J. J.
  • Ecological Society of America
  • DOI: 10.5167/uzh-2060

Invariability of central metabolic flux distribution in Shewanella oneidensis MR-1 under environmental or genetic perturbations
journal, July 2009

  • Tang, Yinjie J.; Martin, Hector Garcia; Deutschbauer, Adam
  • Biotechnology Progress, Vol. 25, Issue 5
  • DOI: 10.1002/btpr.227

From Metaphor to Measurement: Resilience of What to What?
journal, December 2001


Role of apoptosis repressor with caspase recruitment domain (ARC) in cell death and cardiovascular disease
journal, February 2021


First principles of terrestrial life: exemplars for potential extra-terrestrial biology
journal, July 2022


Wastewater treatment high rate algal ponds for biofuel production
journal, January 2011


Rising to the challenge of sustaining coral reef resilience
journal, November 2010

  • Hughes, Terry P.; Graham, Nicholas A. J.; Jackson, Jeremy B. C.
  • Trends in Ecology & Evolution, Vol. 25, Issue 11
  • DOI: 10.1016/j.tree.2010.07.011

Lake microbial communities are resilient after a whole-ecosystem disturbance
journal, June 2012

  • Shade, Ashley; Read, Jordan S.; Youngblut, Nicholas D.
  • The ISME Journal, Vol. 6, Issue 12
  • DOI: 10.1038/ismej.2012.56

Dynamics in microbial communities: unraveling mechanisms to identify principles
journal, December 2014

  • Konopka, Allan; Lindemann, Stephen; Fredrickson, Jim
  • The ISME Journal, Vol. 9, Issue 7
  • DOI: 10.1038/ismej.2014.251

Impact of fire on active layer and permafrost microbial communities and metagenomes in an upland Alaskan boreal forest
journal, April 2014

  • Taş, Neslihan; Prestat, Emmanuel; McFarland, Jack W.
  • The ISME Journal, Vol. 8, Issue 9
  • DOI: 10.1038/ismej.2014.36

Erratum: Corrigendum: Recovery rates reflect distance to a tipping point in a living system
journal, April 2012

  • Veraart, Annelies J.; Faassen, Elisabeth J.; Dakos, Vasilis
  • Nature, Vol. 484, Issue 7394
  • DOI: 10.1038/nature11029

Marine microbial community dynamics and their ecological interpretation
journal, February 2015

  • Fuhrman, Jed A.; Cram, Jacob A.; Needham, David M.
  • Nature Reviews Microbiology, Vol. 13, Issue 3
  • DOI: 10.1038/nrmicro3417

Critical slowing down as early warning for the onset of collapse in mutualistic communities
journal, November 2014

  • Dakos, Vasilis; Bascompte, Jordi
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 49
  • DOI: 10.1073/pnas.1406326111

Slow Recovery from Perturbations as a Generic Indicator of a Nearby Catastrophic Shift
journal, June 2007

  • van Nes, Egbert H.; Scheffer, Marten
  • The American Naturalist, Vol. 169, Issue 6
  • DOI: 10.1086/516845

Highly optimized tolerance: A mechanism for power laws in designed systems
journal, August 1999


Ecological control analysis: being(s) in control of mass flux and metabolite concentrations in anaerobic degradation processes
journal, February 2007


Multiple High-Throughput Analyses Monitor the Response of E. coli to Perturbations
journal, April 2007


The Microbial Engines That Drive Earth's Biogeochemical Cycles
journal, May 2008


Microbial Ecology of Ocean Biogeochemistry: A Community Perspective
journal, May 2008


Predicting a Human Gut Microbiota's Response to Diet in Gnotobiotic Mice
journal, May 2011


Global Resilience of Tropical Forest and Savanna to Critical Transitions
journal, October 2011


Generic Indicators for Loss of Resilience Before a Tipping Point Leading to Population Collapse
journal, May 2012


Microbiome Data Distinguish Patients with Clostridium difficile Infection and Non-C. difficile-Associated Diarrhea from Healthy Controls
journal, May 2014

  • Schubert, Alyxandria M.; Rogers, Mary A. M.; Ring, Cathrin
  • mBio, Vol. 5, Issue 3
  • DOI: 10.1128/mbio.01021-14

Resilience and Stability of Ecological Systems
journal, November 1973


Networked buffering: a basic mechanism for distributed robustness in complex adaptive systems
journal, June 2010

  • Whitacre, James M.; Bender, Axel
  • Theoretical Biology and Medical Modelling, Vol. 7, Issue 1
  • DOI: 10.1186/1742-4682-7-20

Dynamic changes in short- and long-term bacterial composition following fecal microbiota transplantation for recurrent Clostridium difficile infection
journal, March 2015


Microbiota Dynamics in Patients Treated with Fecal Microbiota Transplantation for Recurrent Clostridium difficile Infection
journal, November 2013


Prediction of Metabolic Flux Distribution from Gene Expression Data Based on the Flux Minimization Principle
journal, November 2014


Effects of Biodiversity on Ecosystem Functioning: a Consensus of Current Knowledge
journal, February 2005

  • Hooper, D. U.; Chapin, F. S.; Ewel, J. J.
  • Ecological Monographs, Vol. 75, Issue 1
  • DOI: 10.1890/04-0922

The epsomitic phototrophic microbial mat of Hot Lake, Washington: community structural responses to seasonal cycling
journal, January 2013

  • Lindemann, Stephen R.; Moran, James J.; Stegen, James C.
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00323

Individualized medicine and the microbiome in reproductive tract
journal, April 2015

  • Braundmeier, Andrea G.; Lenz, Katherine M.; Inman, Kristin S.
  • Frontiers in Physiology, Vol. 6
  • DOI: 10.3389/fphys.2015.00097

Mathematical Modeling of Microbial Community Dynamics: A Methodological Review
journal, October 2014

  • Song, Hyun-Seob; Cannon, William; Beliaev, Alexander
  • Processes, Vol. 2, Issue 4
  • DOI: 10.3390/pr2040711

No Vacancy: How Beneficial Microbes Cooperate with Immunity To Provide Colonization Resistance to Pathogens
journal, April 2015

  • Sassone-Corsi, Martina; Raffatellu, Manuela
  • The Journal of Immunology, Vol. 194, Issue 9
  • DOI: 10.4049/jimmunol.1403169

Works referencing / citing this record:

Gut Reactions: Breaking Down Xenobiotic–Microbiome Interactions
journal, February 2019

  • Clarke, Gerard; Sandhu, Kiran V.; Griffin, Brendan T.
  • Pharmacological Reviews, Vol. 71, Issue 2
  • DOI: 10.1124/pr.118.015768

Disentangling the Influence of Environment, Host Specificity and Thallus Differentiation on Bacterial Communities in Siphonous Green Seaweeds
journal, April 2019

  • Morrissey, Kathryn Lee; Çavaş, Levent; Willems, Anne
  • Frontiers in Microbiology, Vol. 10
  • DOI: 10.3389/fmicb.2019.00717

Antibiotic resilience: a necessary concept to complement antibiotic resistance?
journal, December 2019

  • Carvalho, Gabriel; Forestier, Christiane; Mathias, Jean-Denis
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1916
  • DOI: 10.1098/rspb.2019.2408

Community recovery dynamics in yellow perch microbiome after gradual and constant metallic perturbations
journal, February 2020


Engineering microbial consortia for controllable outputs
journal, March 2016

  • Lindemann, Stephen R.; Bernstein, Hans C.; Song, Hyun-Seob
  • The ISME Journal, Vol. 10, Issue 9
  • DOI: 10.1038/ismej.2016.26

Microbial Communities Are Well Adapted to Disturbances in Energy Input
journal, October 2016


Synthetic photosynthetic consortia define interactions leading to robustness and photoproduction
journal, January 2017

  • Hays, Stephanie G.; Yan, Leo L. W.; Silver, Pamela A.
  • Journal of Biological Engineering, Vol. 11, Issue 1
  • DOI: 10.1186/s13036-017-0048-5

Potential and active functions in the gut microbiota of a healthy human cohort
journal, July 2017


A Generalized Spatial Measure for Resilience of Microbial Systems
journal, April 2016

  • Renslow, Ryan S.; Lindemann, Stephen R.; Song, Hyun-Seob
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.00443

Regulation-Structured Dynamic Metabolic Model Provides a Potential Mechanism for Delayed Enzyme Response in Denitrification Process
journal, September 2017


Vancomycin and/or Multidrug-Resistant Citrobacter Freundii Altered the Metabolic Pattern of Soil Microbial Community
journal, May 2018


Functional Diversity of Soil Microbial Communities in Response to the Application of Cefuroxime and/or Antibiotic-Resistant Pseudomonas putida Strain MC1
journal, October 2018

  • Orlewska, Kamila; Markowicz, Anna; Piotrowska-Seget, Zofia
  • Sustainability, Vol. 10, Issue 10
  • DOI: 10.3390/su10103549