Project

Back to overview

Metabolic specialization and the causes of diversity in microbial ecosystems

English title Metabolic specialization and the causes of diversity in microbial ecosystems
Applicant Johnson David Russell
Number 149304
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 01.01.2014 - 31.12.2017
Approved amount 447'101.00
Show all

All Disciplines (2)

Discipline
Experimental Microbiology
Ecology

Keywords (10)

Co-evolution; Microbial communities; Range expansion; Metabolic specialization; Evolutionary ecology; Microbial ecology; Mutualism; Microbial diversity; Tradeoffs; Denitrification

Lay Summary (German)

Lead
Mikrobielle Gemeinschaften beeinflussen die biologischen und chemischen Prozesse nahezu jedes Habitats auf der Erde und bestehen typischerweise aus tausenden verschiedenen Arten. Dieser extrem hohe Grad an Diversität wirft einige der fundamentalsten und herausforderndsten Fragen der mikrobiellen Ökologie auf. Warum bestehen mikrobielle Gemeinschaften aus so vielen Arten? Wie können all diese Arten koexistieren?
Lay summary

Dieses Projekt schlägt drei allgemeingültige Mechanismen vor die Erklären können wie verschiedene Spezies koexistieren: 1) Sie können koexistieren wenn sie verschiedene metabolische Prozesse durchführen, die biochemisch nicht miteinander vereinbar sind. 2) Sie können koexistieren, wenn sie gegenseitig voneinander abhängig sind. 3) Sie können koexistieren wenn sie zusammen koevolviert sind (d.h. wenn evolutionäre Veränderungen in einer Spezies die direkte Antwort auf evolutionäre Veränderungen in einer anderen Spezies sind). Obwohl alle drei Mechanismen durch theoretische Überlegungen gestützt werden, wurde bis jetzt noch keiner experimentell in mikrobiellen Gemeinschaften geprüft. Dieses Projekt schlägt konkrete Experimente vor, um diese Mechanismen zu testen.

Das Testen dieser Mechanismen wird unser grundlegendes Verständnis darüber erweitern, wieso und wie Diversität in mikrobiellen Gemeinschaften entsteht und aufrechterhalten wird. Das Verständnis dieser Prozesse kann wiederum konkrete Anwendungen haben. Man könnte damit zum Beispiel vorhersagen wie metabolische Prozesse auf verschiedene Spezies verteilt werden müssen, um einen gewünschten Biotransformationsprozess optimal ablaufen zu lassen. Somit wird es auch dazu beitragen die Grundlagen für ein neues wissenschaftliches Feld, der synthetischen Ökologie, zu schaffen.

Direct link to Lay Summary Last update: 14.10.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Substrate cross-feeding affects the speed and trajectory of molecular evolution within a synthetic microbial assemblage
LiljaElin, JohnsonDavid (2019), Substrate cross-feeding affects the speed and trajectory of molecular evolution within a synthetic microbial assemblage, in BMC Evolutionary Biology, 19, 129.
Metabolite toxicity slows local diversity loss during expansion of a microbial cross-feeding community
Goldschmidt Felix, Regoes Roland, Johnson David R (2018), Metabolite toxicity slows local diversity loss during expansion of a microbial cross-feeding community, in ISME Journal, 12, 136-144.
A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations
Marchal Marie, Derksen Selina, Panke Sven, Ackermann Martin, Johnson David R (2017), A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations, in BMC Evolutionary Biology, 17, 106.
Metabolite toxicity determines the pace of molecular evolution within microbial populations.
Lilja Elin E, Johnson David R (2017), Metabolite toxicity determines the pace of molecular evolution within microbial populations., in BMC Evolutionary Biology, 17, 52.
Successive range expansion promotes diversity and accelerates evolution in spatially structured microbial populations
Goldschmidt Felix, Regoes Roland, Johnson David R (2017), Successive range expansion promotes diversity and accelerates evolution in spatially structured microbial populations, in ISME Journal, 11, 2112-2123.
Challenges in microbial ecology: building predictive understanding of community function and dynamics
Widder S, Johnson David R (2016), Challenges in microbial ecology: building predictive understanding of community function and dynamics, in ISME Journal, 2557-2568.
Engineering microbial consortia for controllable outputs
Lindemann Stephen, Bernstein Hans, Song Hyun-Seob, Fredrickson Jim, Fields Matthew, Shou Wenying, Johnson David, Beliaev Alexander (2016), Engineering microbial consortia for controllable outputs, in ISME Journal, 2077-2084.
Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates
Lilja Elin, Johnson David (2016), Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates, in ISME Journal, 1568-1578.
Synthetic microbial assemblages and the dynamic interplay between microbial genotypes
Dolinsek Jan, Goldschmidt Felix, Johnson David R (2016), Synthetic microbial assemblages and the dynamic interplay between microbial genotypes, in FEMS Microbiology Reviews, 961-979.
Interaction-dependent effects of surface structure on microbial spatial self-organization
CiccareseDavide, ZuidemaAnita, MerloValeria, JohnsonDavid, Interaction-dependent effects of surface structure on microbial spatial self-organization, in Philosophical Trans Royal Society B, 1.

Collaboration

Group / person Country
Types of collaboration
Theoretical Biology, ETHZ, Prof. Dr. Sebastian Bonhoeffer Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
STEP, ETHZ, Prof. Dr. Dani Or Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure
- Exchange of personnel
Molecular Microbial Ecology, ETHZ, Prof. Dr. Martin Ackermann Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Fundamental Microbiology, Unil, Prof. Dr. Jan Roelof van der Meer Switzerland (Europe)
- Research Infrastructure
- Exchange of personnel

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
14th Symposium on Bacterial Genetics and Ecology Talk given at a conference Evolution of spatial self-organization within denitrifying microbial communities depends on initial frequencies. 04.06.2017 Aberdeen, Scotland, Great Britain and Northern Ireland Goldschmidt Felix; Johnson David Russell;
Scientific Spring Meeting KNVM & NVMM 2017 Talk given at a conference Why does cross-feeding occur within microbial communities? 22.03.2017 Arnhem, Netherlands Johnson David Russell;
16th International Symposium on Microbial Ecology Talk given at a conference Metabolic interactions promote spatial population diversity in expanding microbial populations 21.08.2016 Montreal, Canada Goldschmidt Felix; Johnson David Russell;
6th Swiss Microbial Ecology Meeting Talk given at a conference The causes and consequences of metabolic specialization 10.09.2015 Ascona, Switzerland Lilja Elin; Goldschmidt Felix; Johnson David Russell;
6th Swiss Microbial Ecology Meeting Talk given at a conference The evolution of spatial self-organization in expanding populations of microorganisms 10.09.2015 Ascona, Switzerland Goldschmidt Felix; Johnson David Russell;
15th International Symposium on Microbial Ecology Talk given at a conference When does metabolic specialization lead to more rapid substrate consumption? 24.08.2014 Seoul, Korean Republic (South Korea) Johnson David Russell; Lilja Elin; Goldschmidt Felix;
Understanding Microbial Communities; Function, Structure and Dynamics. Isaac Newton Institute for Mathematical Sciences Talk given at a conference The causes and consequences of metabolic specialization 11.08.2014 Cambridge, Great Britain and Northern Ireland Goldschmidt Felix; Johnson David Russell; Lilja Elin;
1st ASM Conference on Experimental Microbial Evolution Talk given at a conference Hostile environmental conditions accelerate the pace of molecular evolution and niche specialization in bacterial populations 19.06.2014 Washington D.C., United States of America Johnson David Russell; Lilja Elin;
Heraus Seminar: Mechanisms, Strategies, and Evolution of Microbial Systems Talk given at a conference Mutualistic interactions maintain diversity in expanding microbial communities 15.06.2014 Bad Honnef, Germany Goldschmidt Felix; Johnson David Russell;


Associated projects

Number Title Start Funding scheme
176101 The evolutionary and ecological consequences of microbial range expansions 01.01.2018 Project funding (Div. I-III)
132905 Syntrophic Cross-Feeding and the Maintenance of Diversity in Microbial Ecosystems 01.01.2011 Project funding (Div. I-III)

Abstract

Microbial communities impact the biological and chemical processes occurring in nearly every habitat on earth. They are also increasingly called upon to solve some of the most pressing problems facing our society, including the removal of environmental pollutants and the conversion of renewable resources into valuable products. These communities are often tremendously diverse, with a single liter of sea water estimated to contain many thousands of different microbial taxa. These levels of diversity raise some of the most basic and challenging questions in microbial ecology. Why do microbial communities contain so many different cell types? What are the mechanisms that prevent a few cell types from evolving that outcompete the other cell types? Metabolic specialization provides a plausible explanation for how diversity could be promoted and maintained. Consider a microbial cell residing in the human gut. This cell encounters myriad different substrates that could be metabolized to support its growth. Yet, even if this cell were near starvation, it would only metabolize a subset of the available substrates. What is the advantage of metabolizing subsets of the available substrates rather than all of them? What are the underlying causes of metabolic specialization? Can we predict which substrates are likely metabolized by the same cell type and which are likely metabolized by different cell types? We currently lack a deep understanding of the underlying mechanisms causing metabolic specialization, which hinders us from addressing these questions and elucidating the general rules and principles governing the assembly and diversity of microbial communities.In this proposal, I postulate three general mechanisms that could promote and maintain diversity in microbial communities. The first is that incompatibilities between different metabolic processes cause the processes to segregate into different specialized cell types over evolutionary time, thus promoting diversity. Metabolic incompatibilities have often been used to explain the emergence of metabolic specialization, but empirical measures of incompatibilities are limited to a few well-investigated metabolic processes. This hinders us from obtaining a more holistic perspective on metabolic incompatibilities that could reveal the general rules and principles governing the cellular fates of different metabolic processes. To reveal these general rules and principles, I propose specific experiments that address the following critical questions. •Can incompatibilities between hundreds of different pairs of metabolic processes be experimentally measured in parallel, thus generating a more holistic perspective on metabolic incompatibilities?•Are incompatible metabolic processes more likely than compatible metabolic processes to segregate into different specialized cell types, thus promoting diversity?•What are the underlying genetic changes and physiological tradeoffs that cause metabolic specialization and diversification? I also postulate two general mechanisms whereby mutualistic interactions between different metabolically specialized cell types could maintain and promote further diversification in spatially structured environments. The first is that mass transfer limitations of exchanged metabolites constrain the maximum permissible distance between different mutualist cell types, thus maintaining diversity during range expansion. The second is that mutualistic interactions cause co-evolutionary changes between metabolically specialized cell types that promote and maintain diversity during prolonged periods of spatial separation. Although both mechanisms are supported by theoretical considerations, neither has been experimentally tested with microbial communities. To address this knowledge gap, I propose specific experiments that address the following critical questions.•Do mass transfer limitations of exchanged metabolites constrain the maximum permissible distance between different mutualist cell types?•Does this constraint maintain diversity during range expansion?•Do mutualistic interactions cause co-evolutionary changes between metabolically specialized cell types that promote and maintain diversity during prolonged periods of spatial separation?Testing these general mechanisms would significantly advance our basic understanding about why and how diversity is promoted and maintained in microbial communities. Ultimately, the insights gained could be useful for predicting the assembly and diversity of natural microbial communities. The insights also have applied implications. They could be used to predict the optimal distribution of different metabolic processes across different cell types to maximize a desired biotransformation, thus contributing towards establishing a field of synthetic ecology.
-