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The evolutionary and ecological consequences of microbial range expansions

English title The evolutionary and ecological consequences of microbial range expansions
Applicant Johnson David Russell
Number 176101
Funding scheme Project funding (Div. I-III)
Research institution Abteilung für Umweltmikrobiologie EAWAG
Institution of higher education Swiss Federal Institute of Aquatic Science and Technology - EAWAG
Main discipline Experimental Microbiology
Start/End 01.01.2018 - 31.12.2021
Approved amount 426'766.00
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All Disciplines (2)

Discipline
Experimental Microbiology
Ecology

Keywords (8)

Microbial ecology; Cooperation; Spatial ecology; Microbial communities; Range expansion; Denitrification; Evolutionary ecology; Antibiotic resistance

Lay Summary (German)

Lead
Wir untersuchen die Auswirkungen von aufeinanderfolgenden Ausbreitung auf die Ökosystemstabilität und die Ausbreitung von Antibiotikaresistenzen.
Lay summary

Inhalt und Ziele des Forschungsprojekts

Alle Organismen müssen sich irgendwann während ihrer Existenz räumlich ausbreiten. Eine räumliche Ausbreitung tritt auf, wenn eine Population von Organismen in ein noch nicht besiedeltes Gebiet expandiert. Oftmals erfolgt die räumliche Ausbreitung als Abfolge von aufeinanderfolgenden Ausbreitungen, bei welchen eine Population zuerst expandiert und sich eine oder mehrere andere Populationen danach ausbreiten. In der Natur sind räumliche Ausbreitungen allgegenwärtig, über die evolutionären Konsequenzen aufeinanderfolgender Ausbreitung fehlt uns jedoch grundlegendes Wissen.

Das Ziel dieses Projektes ist es, zwei mögliche Konsequenzen der aufeinanderfolgenden Ausbreitung zu testen. Eine Konsequenz könnte sein, dass die aufeinanderfolgende Ausbreitung den Austausch von Genen zwischen verschiedenen Organismen fördert. Ein Beispiel dafür ist der Austausch von
Antibiotikaresistenzgenen zwischen mikrobiellen Populationen im menschlichen Verdauungstrakt. Eine andere Konsequenz könnte sein, dass vorübergehende Schwankungen von Zusammenarbeit und Konflikt zwischen verschiedenen Populationen zu einem Kollaps des Ökosystems führen. Um die Relevanz dieser beiden Konsequenzen testen zu können, wird dieses Projekt ein Modell eines mikrobiellen Ökosystems in Experimenten und mathematischem Modellieren verwenden.

Wissenschaftlicher und gesellschaftlicher Kontext des Forschungsprojekts

Die Ergebnisse dieses Projektes werden unser grundlegendes Verständnis der Konsequenzen der räumlichen Ausbreitung bezüglich ökologischen und evolutionären Prozessen in Populationen verbessern. Insbesondere sollten sie helfen, die Auswirkungen von aufeinanderfolgenden Ausbreitung auf die Ausbreitung von Antibiotikaresistenzen vorherzusagen, was wichtige Auswirkungen darauf haben könnte, wie Antibiotika im klinischen Umfeld angewendet werden.


Direct link to Lay Summary Last update: 14.11.2017

Responsible applicant and co-applicants

Employees

Publications

Publication
Interaction-dependent effects of surface structure on microbial spatial self-organization
Ciccarese Davide, Anita Zuidema, Valeria Merlo, Johnson David R (2020), Interaction-dependent effects of surface structure on microbial spatial self-organization, in Philosophical Transactions of the Royal Society B, 375, 20190246.
Editorial overview: Causes and biotechnological application of microbial metabolic specialization
Johnson David R, Stephan Noack (2020), Editorial overview: Causes and biotechnological application of microbial metabolic specialization, in Current Opinion in Biotechnology, 62, iii-iv.
Substrate cross-feeding affects the speed and trajectory of molecular evolution within a synthetic microbial assemblage
Lilja Elin E., Johnson David R. (2019), Substrate cross-feeding affects the speed and trajectory of molecular evolution within a synthetic microbial assemblage, in BMC Evolutionary Biology, 19(1), 129.
Bridging the Holistic-Reductionist Divide in Microbial Ecology
Tecon Robin, Mitri Sara, Ciccarese Davide, Or Dani, van der Meer Jan Roelof, Johnson David R. (2019), Bridging the Holistic-Reductionist Divide in Microbial Ecology, in mSystems, 4, e00265-18.
Functional microbial landscapes
Ciccarese Davide, Johnson David R (2019), Functional microbial landscapes, in Moo-Young Murray (ed.), Elsevier: Permagon, Amsterdam, 42-51.
Spatial organization in microbial range expansion emerging from trophic dependencies and successful lineages
BorerBenedict, CiccareseDavide, JohnsonDavid, OrDani, Spatial organization in microbial range expansion emerging from trophic dependencies and successful lineages, in Communications Biology, 1.

Collaboration

Group / person Country
Types of collaboration
Prof. Dr. Dani Or - ETH Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Dr. Sara Mitri - Unil Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Dr. Jan Roelof van der Meer - Unil Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Biofilms 9 Talk given at a conference The effect of synthetic microbial spatial self-organization on the fate of antibiotic resistance genes 29.09.2020 Karlsruhe, Germany Johnson David Russell; Ma Yinyin;
Discussion meeting on conflict and cooperation in cellular populations Talk given at a conference Bifurcations and the creation of pattern diversity during microbial spatial self-organization 03.02.2020 Bangalore, India Johnson David Russell;
University of Exeter, Department of Biosciences Individual talk Spatial chaos and the self-organization of microbial communities 07.11.2019 Penryn, England, Great Britain and Northern Ireland Johnson David Russell;
Annual Congress 2019 of the Swiss Society for Microbiology Talk given at a conference Jackpot events prevent ecosystem collapse in the face of environmental fluctuations 03.09.2019 Zurich, Switzerland Merlo Valeria; Zuidema Anita; Johnson David Russell; Ciccarese Davide;
Gordon Research Conference on Microbial Population Biology Poster Consequences of microbial spatial self-organization on horizontal gene transfer 07.07.2019 Andover, NH, United States of America Johnson David Russell; Ma Yinyin;
Gordon Research Seminar on Microbial Population Biology Talk given at a conference Consequences of microbial spatial self-organization on horizontal gene transfer 07.07.2019 Andover, NH, United States of America Ma Yinyin; Johnson David Russell;
8th Congress of European Microbiologists Poster Spatial chaos: can we predict patterns of spatial self-organization within microbial communities? 07.07.2019 Glasgow, Scotland, Great Britain and Northern Ireland Johnson David Russell;
15th Symposium on Bacterial Genetics and Ecology Poster Eco-evolutionary dynamics of ATP-producing pathways in microbial communities 26.05.2019 Lisbon, Portugal Johnson David Russell;
12th Institute of Biogeochemistry and Pollutant Dynamics PhD Congress Poster Evolvability of spatial self-organization during microbial range expansion 26.04.2019 Zurich, Switzerland Johnson David Russell; Ma Yinyin;
12th Institute of Biogeochemistry and Pollutant Dynamics PhD Congress Talk given at a conference Jackpot events prevent ecosystem collapse in the face of environmental fluctuations 26.04.2019 Zurich, Switzerland Ciccarese Davide; Johnson David Russell;
ETH, Evolution of Microbial Sociality Group Individual talk Spatial chaos and the self-organization of microbial communities 03.04.2019 Zurich, Switzerland Johnson David Russell;
7th Swiss Microbial Ecology Meeting Talk given at a conference Effect of fluctuating environmental conditions on spatial self-organization and community stability 30.01.2019 Lausanne, Switzerland Johnson David Russell; Ciccarese Davide;
University of Fribourg, Department of Biology – Ecology and Evolution Individual talk The ecological and evolutionary consequences of microbial range expansions 08.11.2018 Fribourg, Switzerland Johnson David Russell;
European Water Tech Week Leeuwarden 2018 Talk given at a conference Metabolic specialization and the causes of diversity in microbial ecosystems 24.09.2018 Leeuwarden, Netherlands Johnson David Russell;
17th International Symposium on Microbial Ecology Poster Division of labor in sequential metabolic processes; an eco-evolutionary perspective 12.08.2018 Leipzig, Germany Johnson David Russell;
17th International Symposium on Microbial Ecology Poster Effect of fluctuating environmental conditions on spatial self-organization and community stability 12.08.2018 Leipzig, Germany Ciccarese Davide; Johnson David Russell;
17th International Symposium on Microbial Ecology Talk given at a conference Spatial chaos: Can we predict patterns of spatial self-organization within microbial communities? 12.08.2018 Leipzig, Germany Johnson David Russell;
Biofilms 8 Talk given at a conference Effect of fluctuating environmental conditions on the spatial self-organization and emergent properties of a synthetic microbial biofilm 27.05.2018 Aarhus, Denmark Ciccarese Davide; Johnson David Russell;
University of Geneva, Department of Microbiology and Molecular Medicine Individual talk The ecological and evolutionary consequences of microbial range expansions 23.05.2018 Geneva, Switzerland Johnson David Russell;
Microbiology Society Annual Conference 2018 Talk given at a conference The ecological and evolutionary consequences of microbial range expansions 10.04.2018 Birmingham, England, Great Britain and Northern Ireland Johnson David Russell;


Associated projects

Number Title Start Funding scheme
149304 Metabolic specialization and the causes of diversity in microbial ecosystems 01.01.2014 Project funding (Div. I-III)

Abstract

A vast amount of the natural microbial world lives attached to surfaces, such as the microbial communities residing in the human gut, in soil ecosystems, or on particulate matter in the open ocean. An inherent behavior of surface-attached microbial communities is that they must, at some point in their existence, undergo range expansion. A range expansion occurs when microbial communities expand into previously unoccupied space. Range expansions likely occur as a series of successive expansions, where one microbial strain expands first (the primary expansion) and one or more other microbial strains expand afterwards (secondary expansions). While successive range expansions are pervasive in nature, the consequences of successive range expansions remain poorly understood. How might successive range expansions affect the evolutionary processes acting on microbial communities? How might they affect the ecological functioning and stability of microbial communities? In this proposal, I postulate two potentially general consequences of successive range expansions. The first is that successive range expansions should promote the transfer of genes between different microbial strains, such as the transfer of antibiotic resistance genes in the human gut. The main hypothesis is that successive range expansions increase the number of cell-cell contacts between different strains, thus increasing the probability of gene transfer between those strains. To address this hypothesis, I propose specific experiments to address the following questions:•Do successive range expansions promote the transfer of genes between different microbial strains?•After acquiring beneficial genes, can recipient cells proliferate and establish within a successive range expansion? •How does the magnitude of benefits bestowed by newly acquired genes affect the proliferation and establishment of recipient cells?The second consequence is that temporal fluctuations between cooperation and conflict between different microbial strains during range expansions may cause ecosystems to collapse. The main hypothesis is that cooperation and conflict promote the emergence of different spatial cell arrangements, and these spatial cell arrangements are in conflict with each other (i.e. the arrangements that emerge during cooperation are detrimental during competition and vice versa). Fluctuations between cooperation and conflict may therefore destabilize ecosystems and promote their eventual collapse. To address this hypothesis, I propose specific experiments to address the following questions: •Do temporal fluctuations between cooperation and conflict promote the eventual collapse of ecosystems during range expansions?•Do feedbacks emerge that mitigate the destabilizing effects of such temporal fluctuations, thus slowing or preventing ecosystem collapse?•If ecosystems escape collapse, what are the mechanisms that enable escape?Together, answering these questions will significantly advance our basic understanding about the evolutionary and ecological consequences of microbial range expansions. Given that every surface-attached microbial community must undergo range expansions, the insights gained will be of potential importance for nearly any surface-attached microbial community, including those important for the environment, biotechnology, and human health and disease.
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