Ecological Stability Properties of Microbial Communities Assessed by Flow Cytometry

ABSTRACT Natural microbial communities affect human life in countless ways, ranging from global biogeochemical cycles to the treatment of wastewater and health via the human microbiome. In order to probe, monitor, and eventually control these communities, fast detection and evaluation methods are re...

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Autores principales: Zishu Liu, Nicolas Cichocki, Fabian Bonk, Susanne Günther, Florian Schattenberg, Hauke Harms, Florian Centler, Susann Müller
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:2beaa2d1778843ca9001548d4ef255d52021-11-15T15:22:01ZEcological Stability Properties of Microbial Communities Assessed by Flow Cytometry10.1128/mSphere.00564-172379-5042https://doaj.org/article/2beaa2d1778843ca9001548d4ef255d52018-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00564-17https://doaj.org/toc/2379-5042ABSTRACT Natural microbial communities affect human life in countless ways, ranging from global biogeochemical cycles to the treatment of wastewater and health via the human microbiome. In order to probe, monitor, and eventually control these communities, fast detection and evaluation methods are required. In order to facilitate rapid community analysis and monitor a community’s dynamic behavior with high resolution, we here apply community flow cytometry, which provides single-cell-based high-dimensional data characterizing communities with high acuity over time. To interpret time series data, we draw inspiration from macroecology, in which a rich set of concepts has been developed for describing population dynamics. We focus on the stability paradigm as a promising candidate to interpret such data in an intuitive and actionable way and present a rapid workflow to monitor stability properties of complex microbial ecosystems. Based on single-cell data, we compute the stability properties resistance, resilience, displacement speed, and elasticity. For resilience, we also introduce a method which can be implemented for continuous online community monitoring. The proposed workflow was tested in a long-term continuous reactor experiment employing both an artificial and a complex microbial community, which were exposed to identical short-term disturbances. The computed stability properties uncovered the superior stability of the complex community and demonstrated the global applicability of the protocol to any microbiome. The workflow is able to support high temporal sample densities below bacterial generation times. This may provide new opportunities to unravel unknown ecological paradigms of natural microbial communities, with applications to environmental, biotechnological, and health-related microbiomes. IMPORTANCE Microbial communities drive many processes which affect human well-being directly, as in the human microbiome, or indirectly, as in natural environments or in biotechnological applications. Due to their complexity, their dynamics over time is difficult to monitor, and current sequence-based approaches are limited with respect to the temporal resolution. However, in order to eventually control microbial community dynamics, monitoring schemes of high temporal resolution are required. Flow cytometry provides single-cell-based data in the required temporal resolution, and we here use such data to compute stability properties as easy to interpret univariate indicators of microbial community dynamics. Such monitoring tools will allow for a fast, continuous, and cost-effective screening of stability states of microbiomes. Applicable to various environments, including bioreactors, surface water, and the human body, it will contribute to the development of control schemes to manipulate microbial community structures and performances.Zishu LiuNicolas CichockiFabian BonkSusanne GüntherFlorian SchattenbergHauke HarmsFlorian CentlerSusann MüllerAmerican Society for Microbiologyarticleconstancymicrobial communitiesmicrobial ecologymicrobial flow cytometryresilienceresistanceMicrobiologyQR1-502ENmSphere, Vol 3, Iss 1 (2018)
institution DOAJ
collection DOAJ
language EN
topic constancy
microbial communities
microbial ecology
microbial flow cytometry
resilience
resistance
Microbiology
QR1-502
spellingShingle constancy
microbial communities
microbial ecology
microbial flow cytometry
resilience
resistance
Microbiology
QR1-502
Zishu Liu
Nicolas Cichocki
Fabian Bonk
Susanne Günther
Florian Schattenberg
Hauke Harms
Florian Centler
Susann Müller
Ecological Stability Properties of Microbial Communities Assessed by Flow Cytometry
description ABSTRACT Natural microbial communities affect human life in countless ways, ranging from global biogeochemical cycles to the treatment of wastewater and health via the human microbiome. In order to probe, monitor, and eventually control these communities, fast detection and evaluation methods are required. In order to facilitate rapid community analysis and monitor a community’s dynamic behavior with high resolution, we here apply community flow cytometry, which provides single-cell-based high-dimensional data characterizing communities with high acuity over time. To interpret time series data, we draw inspiration from macroecology, in which a rich set of concepts has been developed for describing population dynamics. We focus on the stability paradigm as a promising candidate to interpret such data in an intuitive and actionable way and present a rapid workflow to monitor stability properties of complex microbial ecosystems. Based on single-cell data, we compute the stability properties resistance, resilience, displacement speed, and elasticity. For resilience, we also introduce a method which can be implemented for continuous online community monitoring. The proposed workflow was tested in a long-term continuous reactor experiment employing both an artificial and a complex microbial community, which were exposed to identical short-term disturbances. The computed stability properties uncovered the superior stability of the complex community and demonstrated the global applicability of the protocol to any microbiome. The workflow is able to support high temporal sample densities below bacterial generation times. This may provide new opportunities to unravel unknown ecological paradigms of natural microbial communities, with applications to environmental, biotechnological, and health-related microbiomes. IMPORTANCE Microbial communities drive many processes which affect human well-being directly, as in the human microbiome, or indirectly, as in natural environments or in biotechnological applications. Due to their complexity, their dynamics over time is difficult to monitor, and current sequence-based approaches are limited with respect to the temporal resolution. However, in order to eventually control microbial community dynamics, monitoring schemes of high temporal resolution are required. Flow cytometry provides single-cell-based data in the required temporal resolution, and we here use such data to compute stability properties as easy to interpret univariate indicators of microbial community dynamics. Such monitoring tools will allow for a fast, continuous, and cost-effective screening of stability states of microbiomes. Applicable to various environments, including bioreactors, surface water, and the human body, it will contribute to the development of control schemes to manipulate microbial community structures and performances.
format article
author Zishu Liu
Nicolas Cichocki
Fabian Bonk
Susanne Günther
Florian Schattenberg
Hauke Harms
Florian Centler
Susann Müller
author_facet Zishu Liu
Nicolas Cichocki
Fabian Bonk
Susanne Günther
Florian Schattenberg
Hauke Harms
Florian Centler
Susann Müller
author_sort Zishu Liu
title Ecological Stability Properties of Microbial Communities Assessed by Flow Cytometry
title_short Ecological Stability Properties of Microbial Communities Assessed by Flow Cytometry
title_full Ecological Stability Properties of Microbial Communities Assessed by Flow Cytometry
title_fullStr Ecological Stability Properties of Microbial Communities Assessed by Flow Cytometry
title_full_unstemmed Ecological Stability Properties of Microbial Communities Assessed by Flow Cytometry
title_sort ecological stability properties of microbial communities assessed by flow cytometry
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/2beaa2d1778843ca9001548d4ef255d5
work_keys_str_mv AT zishuliu ecologicalstabilitypropertiesofmicrobialcommunitiesassessedbyflowcytometry
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AT susannegunther ecologicalstabilitypropertiesofmicrobialcommunitiesassessedbyflowcytometry
AT florianschattenberg ecologicalstabilitypropertiesofmicrobialcommunitiesassessedbyflowcytometry
AT haukeharms ecologicalstabilitypropertiesofmicrobialcommunitiesassessedbyflowcytometry
AT floriancentler ecologicalstabilitypropertiesofmicrobialcommunitiesassessedbyflowcytometry
AT susannmuller ecologicalstabilitypropertiesofmicrobialcommunitiesassessedbyflowcytometry
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