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Syntrophic Cross-Feeding and the Maintenance of Diversity in Microbial Ecosystems

English title Syntrophic Cross-Feeding and the Maintenance of Diversity in Microbial Ecosystems
Applicant Johnson David Russell
Number 132905
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 01.01.2011 - 31.12.2013
Approved amount 288'000.00
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All Disciplines (3)

Discipline
Experimental Microbiology
Ecology
Environmental Research

Keywords (11)

Microbial ecosystems; Microbial diversity; Diversification; Cross-feeding; Syntrophy; Trade-offs; Coevolution; Denitrification; Microbial Ecology; Biodiversity; Evolutionary Ecology

Lay Summary (English)

Lead
Lay summary
Microbial communities impact the biological and chemical processes occurring in nearly every habitat on earth and are increasingly being called upon to solve some of the most pressing problems facing our society. These communities are often tremendously diverse, with a single gram of soil estimated to contain thousands to millions of different microbial species. These levels of diversity appear to conflict with the predictions of the competitive exclusion principle, which states that two species that utilize the same resource cannot coexist in a constant environment. This raises two of the most challenging questions in microbial ecology. First, how can so many microbial species coexist in the environment? In other words, what maintains these levels of diversity in the face of competitive exclusion? Second, how are all these species assembled within a community? Thus far, we lack general principles that can be used to address these types of questions.Cross-feeding is a widely observed assembly phenomenon that, at the surface, appears to conflict with the competitive exclusion principle. Cross-feeding occurs when the complete degradation of a single energy-yielding substrate is partitioned between two or more microorganisms, where one microorganism partially degrades a substrate to intermediates and other microorganisms then further degrade the intermediates. Why would a microorganism only partially degrade a substrate? Why don't completely degrading microorganisms always outcompete cross-feeding microorganisms? Under what biological and environmental conditions is cross-feeding a likely evolutionary outcome? These questions have yet to be fully answered. The objective of this research is to understand why cross-feeding sometimes emerges in microbial communities. To address these questions, this work proposes to investigate cross-feeding using respiratory denitrification in the bacterium Pseudomonas stutzeri. Mutants of P. stutzeri with different denitrification capabilities will be constructed, assembled into cross-feeding consortia, and experimentally investigated to accomplish the following specific goals. o Derive and experimentally test general principles that predict when cross-feeding is likely to emerge from a single population of complete denitrifiers. o Test if coevolutionary changes occur during the evolution of syntrophic cross-feeding microorganisms and determine if coevolutionary changes act as barriers to gene flow. Achieving these two goals will help us to better understand how microorganisms are assembled within communities and how diversity is maintained in the face of competitive exclusion.
Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
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.
Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates
Lilja Elin E, Johnson David R (2016), Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates, in ISME Journal, 10, 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, 40, 961-979.
Engineering microbial consortia for controllable outputs
Lindemann Steven R, Bernstein H C, Song H S, Fredrickson J K, Fields M W, Shou W, Johnson David R, Beliaev A S (2015), Engineering microbial consortia for controllable outputs, in ISME Journal, 2077-2084.
Metabolic specialization and the assembly of microbial communities
Johnson Davd R., Goldschmidt Felix, Lilja Elin E., Ackermann M (2012), Metabolic specialization and the assembly of microbial communities, in ISME Journal, 6, 902-904.
A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations
Marchal Marie, Derksen Selina, Panke Sven, Ackermann Martin, Johnson David R, A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations, in BMC Evolutionary Biology.
Successive range expansion promotes diversity and accelerates evolution in spatially structured microbial populations
Goldschmidt Felix, Regoes Roland, Johnson David R, Successive range expansion promotes diversity and accelerates evolution in spatially structured microbial populations, in ISME Journal.

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
EMBL: New Approaches and Concepts in Microbiology Poster Mutualistic coevolution promotes diversification in populations of cross-feeding microorganisms 14.10.2013 Heidelberg, Germany Johnson David Russell; Lilja Elin;
Departmental Seminar Individual talk Metabolic specialization and the causes of diversity in microbial ecosystems 05.04.2013 University of Colorado, United States of America Johnson David Russell;
Departmental Seminar Individual talk Metabolic specialization and the causes of diversity in microbial ecosystems 04.04.2013 Colorado School of Mines, United States of America Johnson David Russell;
Departmental Seminar Individual talk Metabolic specialization and the causes of diversity in microbial ecosystems 15.02.2013 Yonsei University, Korean Republic (South Korea) Johnson David Russell;
Departmental Seminar Individual talk Metabolic incompatibilities promote diversification in microbial populations 11.02.2013 Aquatic Ecology, Eawag, Switzerland, Switzerland Johnson David Russell;
5th Meeting of the Swiss Microbial Ecology Group Talk given at a conference Mutualistic interactions maintain diversity in expanding microbial communities. 04.02.2013 Murten, Switzerland Goldschmidt Felix; Johnson David Russell;
14th International Symposium on Microbial Ecology Poster Cross-feeding interactions shape the spatial arrangement of denitrifying microbial communities 20.08.2012 Copenhagen, Denmark Johnson David Russell; Goldschmidt Felix;
14th International Symposium on Microbial Ecology Poster Adaptive evolution of Pseudomonas stutzeri under denitrifying conditions 20.08.2012 Copenhagen, Denmark Johnson David Russell; Lilja Elin;
4th Congress of European Microbiologists FEMS Talk given at a conference The emergence of cross-feeding within populations of denitrifying bacteria 26.06.2011 Geneva, Switzerland, Switzerland Johnson David Russell;
111th General Meeting of the American Society for Microbiology Talk given at a conference The emergence of cross-feeding within populations of denitrifying bacteria 21.05.2011 New Orleans, LA, USA, United States of America Johnson David Russell;
Mathematics of Microbes: Biological Details of the Evolving Cell Talk given at a conference Cross-feeding and the spatial arrangement of microbial communities 27.04.2011 Imperial College, London, UK, Great Britain and Northern Ireland Johnson David Russell;
4th Meeting of the Swiss Microbial Ecology Group Talk given at a conference Why does cross-feeding occur within microbial communities? 02.02.2011 Engelberg, Switzerland 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

Microbial communities impact the biological and chemical processes occurring in nearly every habitat on earth and are increasingly being called upon to solve some of the most pressing problems facing our society. These communities are often tremendously diverse, with a single gram of soil estimated to contain thousands to millions of different microbial species. These levels of diversity appear to conflict with the predictions of the competitive exclusion principle, which states that two species that utilize the same resource cannot coexist in a constant environment. This raises two of the most challenging questions in microbial ecology. First, how can so many microbial species coexist in the environment? In other words, what maintains these levels of diversity in the face of competitive exclusion? Second, how are all these species assembled within a community? Thus far, we lack general principles that can be used to address these types of questions.Cross-feeding is a widely observed assembly phenomenon that, at the surface, appears to conflict with the competitive exclusion principle. Cross-feeding occurs when the complete degradation of a single energy-yielding substrate is partitioned between two or more microorganisms, where one microorganism partially degrades a substrate to intermediates and other microorganisms then further degrade the intermediates. Why would a microorganism only partially degrade a substrate? Why don’t completely degrading microorganisms always outcompete cross-feeding microorganisms? Under what biological and environmental conditions is cross-feeding a likely evolutionary outcome? These questions have yet to be fully answered. In addition to being an important assembly phenomenon, cross-feeding can drive microbial diversification by several processes. The first is the emergence of cross-feeding itself from a single population of completely degrading microorganisms. The second results from coevolutionary changes in syntrophic cross-feeding partners during periods of restricted gene flow. Both of these processes can act in the absence of abiotic variation, and may therefore help explain how microbial diversity is maintained in the face of competitive exclusion. Our understanding of these processes, however, is limited by a lack of laboratory cross-feeding systems that are well defined and experimentally tractable. Developing robust experimental systems would allow for a better understanding of the relevance of these processes to microbial diversification.My primary interest is in the evolution and biological significance of syntrophic cross-feeding. I want to know why cross-feeding sometimes emerges in microbial communities and if there are general principles that predict when cross-feeding is a likely evolutionary outcome. I also want to know how cross-feeding contributes to the maintenance of diversity in microbial communities. I propose to investigate syntrophic cross-feeding using respiratory denitrification in the bacterium Pseudomonas stutzeri. I am currently constructing mutants of P. stutzeri with different denitrification capabilities, assembling them into cross-feeding consortia, and testing their biological behavior. Using this experimental system, I seek to accomplish the following specific goals.•Derive and experimentally test general principles that predict when cross-feeding is likely to emerge from a single population of complete denitrifiers. Based upon theoretical investigations that I performed with the denitrification pathway, I predict that biochemical constraints limiting the maximal activities of different denitrification steps determine if cross-feeding is a likely evolutionary outcome. I now seek to experimentally test this prediction by measuring these constraints and comparing the performance of cross-feeding and completely denitrifying strains under different environmental conditions. •Test if coevolutionary changes occur during the evolution of syntrophic cross-feeding microorganisms and determine if coevolutionary changes act as barriers to gene flow. I will first experimentally evolve cross-feeding strains together in the laboratory and then test if beneficial mutations arise in one cross-feeding strain in direct response to mutations in its syntrophic cross-feeding partner. I will then evaluate if these coevolutionary changes result in incompatibilities between different lineages of evolved cross-feeding strains, and thus potentially act as barriers to gene flow.Achieving these two goals will help us to better understand how microorganisms are assembled within communities and how diversity is maintained in the face of competitive exclusion. Ultimately, the insights gained from this research should be useful for predicting the behavior and assembly of microbial communities in the environment. This research also has implications for applied microbiology and biotechnology. The insights gained could be used to predict the optimal assembly of a microbial community such that the efficiency of a desired process is maximized.
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