Phenotypic innovation through recombination in genome-scale metabolic networks.
Recombination is an important source of metabolic innovation, especially in prokaryotes, which have evolved the ability to survive on many different sources of chemical elements and energy. Metabolic systems have a well-understood genotype-phenotype relationship, which permits a quantitative and biochemically principled understanding of how recombination creates novel phenotypes. Here, we investigate the power of recombination to create genome-scale metabolic reaction networks that enable an organism to survive in new chemical environments. To this end, we use flux balance analysis, an experimentally validated computational method that can predict metabolic phenotypes from metabolic genotypes. We show that recombination is much more likely to create novel metabolic abilities than random changes in chemical reactions of a metabolic network. We also find that phenotypic innovation is more likely when recombination occurs between parents that are genetically closely related, phenotypically highly diverse, and viable on few rather than many carbon sources. Survival on a new carbon source preferentially involves reactions that are superessential, that is, essential in many metabolic networks. We validate our observations with data from 61 reconstructed prokaryotic metabolic networks. Our systematic and quantitative analysis of metabolic systems helps understand how recombination creates innovation.
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Building Y27, Winterthurerstrasse 190, 8057 Zurich, Switzerland The Swiss Institute of Bioinformatics, Quartier Sorge, Batiment Genopode, 1015 Lausanne, Switzerland.
Sayed-Rzgar
http://orcid.org/0000-0002-2308-6754
SR
Hosseini
GQE-Le Moulon, INRA, Université Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91190 Gif-sur-Yvette, France.
Olivier C
OC
Martin
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Building Y27, Winterthurerstrasse 190, 8057 Zurich, Switzerland The Swiss Institute of Bioinformatics, Quartier Sorge, Batiment Genopode, 1015 Lausanne, Switzerland The Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA andreas.wagner@ieu.uzh.ch.
Andreas
A
Wagner
genome-scale metabolic networks; metabolic genotype; metabolic innovation; metabolic phenotype; recombination; superessential reactions
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