Co-evolution; Microbial communities; Range expansion; Metabolic specialization; Evolutionary ecology; Microbial ecology; Mutualism; Microbial diversity; Tradeoffs; Denitrification
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.
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.
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.
Lilja Elin E, Johnson David R (2017), Metabolite toxicity determines the pace of molecular evolution within microbial populations., in BMC Evolutionary Biology
, 17, 52.
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.
Widder S, Johnson David R (2016), Challenges in microbial ecology: building predictive understanding of community function and dynamics, in ISME Journal
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
Lilja Elin, Johnson David (2016), Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates, in ISME Journal
Dolinsek Jan, Goldschmidt Felix, Johnson David R (2016), Synthetic microbial assemblages and the dynamic interplay between microbial genotypes, in FEMS Microbiology Reviews
CiccareseDavide, ZuidemaAnita, MerloValeria, JohnsonDavid, Interaction-dependent effects of surface structure on microbial spatial self-organization, in Philosophical Trans Royal Society B
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.