Adaptive evolution of complex innovations through stepwise metabolic niche expansion

Balázs Szappanos, Jonathan Fritzemeier, Bálint Csörgő, Viktória Lázár, Xiaowen Lu, Gergely Fekete, Balázs Bálint, Róbert Herczeg, István Nagy, Richard A. Notebaart, Martin J. Lercher, Csaba Pál () and Balázs Papp ()
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Balázs Szappanos: Synthetic and Systems Biology Unit, Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences
Jonathan Fritzemeier: Heinrich Heine University, Universitätsstraße 1
Bálint Csörgő: Synthetic and Systems Biology Unit, Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences
Viktória Lázár: Synthetic and Systems Biology Unit, Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences
Xiaowen Lu: Radboud University Medical Centre
Gergely Fekete: Synthetic and Systems Biology Unit, Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences
Balázs Bálint: SeqOmics Biotechnology Ltd
Róbert Herczeg: SeqOmics Biotechnology Ltd
István Nagy: SeqOmics Biotechnology Ltd
Richard A. Notebaart: Radboud University Medical Centre
Martin J. Lercher: Heinrich Heine University, Universitätsstraße 1
Csaba Pál: Synthetic and Systems Biology Unit, Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences
Balázs Papp: Synthetic and Systems Biology Unit, Institute of Biochemistry, Biological Research Centre of the Hungarian Academy of Sciences

Nature Communications, 2016, vol. 7, issue 1, 1-10

Abstract: Abstract A central challenge in evolutionary biology concerns the mechanisms by which complex metabolic innovations requiring multiple mutations arise. Here, we propose that metabolic innovations accessible through the addition of a single reaction serve as stepping stones towards the later establishment of complex metabolic features in another environment. We demonstrate the feasibility of this hypothesis through three complementary analyses. First, using genome-scale metabolic modelling, we show that complex metabolic innovations in Escherichia coli can arise via changing nutrient conditions. Second, using phylogenetic approaches, we demonstrate that the acquisition patterns of complex metabolic pathways during the evolutionary history of bacterial genomes support the hypothesis. Third, we show how adaptation of laboratory populations of E. coli to one carbon source facilitates the later adaptation to another carbon source. Our work demonstrates how complex innovations can evolve through series of adaptive steps without the need to invoke non-adaptive processes.

Date: 2016
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DOI: 10.1038/ncomms11607

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