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The selective cause of an ancient adaptation
Guoping Zhu1, G Brian Golding, Antony M Dean
1BioTechnology Institute, University of Minnesota, St. Paul, MN 55108, USA.
Science (New York, N.Y.)
|January 18, 2005
Summary
Prokaryotic isocitrate dehydrogenase (IDH) evolved NADP dependence early in Earth's history. This adaptation aids anabolic demands during acetate metabolism, particularly when other reduced NADP sources are absent.
Area of Science:
- Biochemistry
- Evolutionary Biology
- Microbial Metabolism
Background:
- The cofactor dependency of key metabolic enzymes provides insights into evolutionary history.
- Isocitrate dehydrogenase (IDH) exists in NAD-dependent and NADP-dependent forms, with distinct roles in prokaryotes and eukaryotes.
- The evolutionary origin of NADP-dependent IDH in prokaryotes coincides with the emergence of eukaryotic mitochondria.
Purpose of the Study:
- To investigate the evolutionary origin and functional significance of NADP-dependent prokaryotic isocitrate dehydrogenase (IDH).
- To determine the selective pressures favoring NADP-dependent IDH in prokaryotic metabolism, particularly during growth on acetate.
Main Methods:
- Phylogenetic analysis of IDH evolution and cofactor usage.
- Genetic engineering of Escherichia coli to replace wild-type NADP-dependent IDH with an ancestral NAD-dependent variant.
- Competitive growth assays using engineered E. coli strains under varying metabolic conditions, including acetate utilization and depletion of alternative reduced NADP sources.
Main Results:
- Phylogenetic analysis suggests NADP-dependent IDH emerged around 3.5 billion years ago, coinciding with mitochondrial appearance.
- Engineered NAD-dependent IDH conferred a competitive disadvantage, especially when alternative sources of reduced nicotinamide adenine dinucleotide phosphate (NADP) were removed.
- Genomic surveys revealed a strong correlation: prokaryotes utilizing acetate via isocitrate lyase exclusively possess NADP-dependent IDH, while those with only NAD-dependent IDH lack isocitrate lyase.
Conclusions:
- The NADP dependence of prokaryotic IDH is an ancient adaptation, not merely a relic.
- This adaptation is specifically linked to meeting the anabolic demand for reduced NADP during growth on acetate.
- The evolutionary trajectory of IDH cofactor preference is intertwined with microbial metabolic strategies and the early evolution of cellular respiration.
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